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BASHFORD DEAN MEMORIAL VOLUME
ENRCIGUEME lelislales
Edited By IQ. 4
EUGENE WILLIS GUDGER
Part Il
TABLE OF CONTENTS
ARTICLES VI, VII, VIII
AND
ANALYTICAL SUBJECT INDEX
NATURAL
STO
N /
K aN AG
Ww Al y
NIX y) SCIENCE y
< 01 Y
NEW YORK
PUBLISHED BY ORDER OF THE TRUSTEES
1937-1942
43-15 5469- Oa . 26
ARTICLE
VI
VII
VIII
PART II
WABEEVOEVEONMENTS
Bertram G. SmitTH
THe ANATOMY OF THE FRILLED SHARK, CHLAMYDOSELACHUS ANGUINEUS
Plate I-VI, text-figures 1-128, pages 331-520.
E. W. GupGER
THE Breepine Hasirs, REPRODUCTIVE ORGANS AND ExTERNAL EMBRYONIC
DEVELOPMENT OF CHLAMYDOSELACHUS BaAsED ON Notes AND DRAWINGS
BY BAsHFORD DEAN
Plates LVI, text-figures 1-33, pages 521-646.
BERTRAM G. SMITH
THE HETERODONTID SHARKS: THEIR NatTurAL History AND THE
ExtERNAL DEVELOPMENT OF HETERODONTUS JAPONICUS BaAsED ON NOTES
AND Drawinecs By BAsHFORD DEAN
Plates I-VII, text-figures 1-69, pages 647-784.
ANALYTICAL SuBJECT INDEX
Ill
PAGE
331
521
647
785
Reprinted from THe AMERICAN NATURALIST, Vol. LXXX, No. 794,
pages 579-583, September—October, 1946.
OBITUARY
BERTRAM GARNER SMITH, 1876-1945
DR. E. W. GUDGER
AMERICAN MusbUM or NATURAL HISTORY
Dr. SmirH was born October 7, 1876, at Painesville,
Ohio, the son of Albert W. and Hlla Garner Smith. He
died of a heart attack at his home in Albuquerque, N. M.,
July 30,1945. He is survived by his wife and a daughter.
He was of New England ancestry, through his grand-
mother Smith, from the Mortons who settled New Salem,
Mass., about 1660.
When Smith was about two years old, his parents
moved to Youngsville, Warren Co., northwestern Penn-
sylvania. There he received his early education, gradu-
ating from high school in 1893. In 1894, he entered the
Pennsylvania State Normal School at Edinboro and
graduated in 1896. For the next two years he taught
in the public grade schools of his section of Pennsylvania.
From 1899 to 1902, during the winters, he taught the
sciences in the High Schools of Warren, Dubois, and
Corry, Pa., and between times attended the summer ses-
sions of Cornell University. In 1903, he matriculated at
the University of Michigan, where he was assistant in
zoology to Professor J. EK. Reighard 1904-07, and from
which he graduated A.B. in 1907.
He was instructor in biology at Lake Forest College
in the spring of 1907, in zoology at Syracuse University
1907-09, and at Wisconsin in 1909-11. In 1911, he
entered Columbia University as a graduate student in
zoology under Dr. Bashford Dean, and because of much
published research, he was able to take his Ph.D. in 1912.
From this year’s work stemmed a lifelong friendship
with Dr. Dean. From 1912-16, he was assistant profes-
sor of zoology at Michigan State Normal College and
associate professor 1916-21. From 1921 to 1930 he was
associate professor of anatomy in New York University
579
580 - THE AMERICAN NATURALIST [Vol. LXXX
BERTRAM GARNER SMITH
No. 794] BERTRAM GARNER SMITH 581
Medical College and professor of anatomy from 1930
until his retirement in September 1942.
Over the years 1906-1929, Smith’s scientific work was
chiefly done on amphibians. Of his 49 published papers,
22 were on members of this group, and 13 of these dealt
with the giant salamander, Cryptobranchus alleghenien-
sis. His interest in this dates from boyhood, when, fish-
ing in the stream near his home, he would frequently
eateh a Cryptobranchus instead of a fish. Thus, when
he learned of the importance of this animal from a zoo-
logical point of view, he knew where to find it. The
breeding season and habits of this amphibian, sought for
almost a generation, were a mystery until it was discoy-
ered that, unlike other amphibians, it breeds not in the
spring but in the fall. Smith studied its habits and
found how oviposition and fertilization are effected. His
field observations ranged from 1905-1911, and his labora-
tory work from 1906-1929.
The difficulties of the field work of collecting and ‘‘fix-
ing’’ the egg and life history stages were great. But
quite as great were those of the laboratory work of em-
bedding and sectioning these yolk-laden amphibian ege's
averaging 6.2 mm. in diameter and exceeded in size only
by those of C. japonicus (c. 7 mm. in diameter). Smith
was a good artist and his papers are illustrated by his
own drawings and photographs. The work on his
articles, from start to finish, was done with his own hands.
Unlike many researchers, he never had the help of assis-
tants.
Smith’s thirteen papers on the natural history and em-
bryology of Cryptobranchus (published mainly in the
Biological Bulletin and Journal of Morphology), range
in date from 1906-1929. They comprise 484 pages and
590 drawings and photographs. Hven a general exami-
nation of his papers on Cryptobranchus reveals what a
prodigious amount of meticulous histological work he did
on the development stages of these huge eggs and early
embryos. I do not recall any vertebrate whose natural
582 THE AMERICAN NATURALIST [Vol. LXXxX
history and embryology have been more thoroughly and
successfully studied. These studies, together with those
on Amblystoma and Necturus, comprise the major inter-
est of the first period of his scientific activities.
The second period of Smith’s productive scientific work
began shortly after the death (December 6, 1928) of his
_ teacher at Columbia, Dr. Bashford Dean. An organiza-
tion of Dr. Dean’s associates, students, friends and fam-
ily was set up to establish memorials to him. Bronze
plaques were cast and mounted in the American and
Metropolitan Museums. Then came the question of what
to do with four sets of splendid drawings (some in color)
of certain archaic fishes—myxinoids and sharks—made
for reproduction by lithography, and it was decided that
these should be published as a Memorial Atlas under the
direction of Dr. Smith and the writer (as editor).
After much thought, I determined that, instead of a
Memorial Atlas, we would publish a Memorial Volume
if I could have Smith’s help, since his training in embry-
ology and anatomy would be invaluable. And when next
he came to my office, I announced my proposed plan and
without a moment’s hesitation he held out his hand and
said—‘I came to tell you just that thing. I, too, owe it
to Dr. Dean.’’ Nothing more clearly illustrates the spirit
of theman. Then began work that covered 13 years and
in which we did five of the eight articles in the volume.
This was especially hard for Smith, who was carrying a
full teaching load in the department of anatomy of New
York University Medical College. Furthermore, it was
time-consuming for him to come to and return from the
American Museum. But for all that—he came.
In 1931 and 1933, we published two joint papers—one
on the natural history of the frilled shark. Then came
the long hard pull for more than three years in which
Smith prepared his great ‘‘ Anatomy of the Frilled Shark,
Chlamydoselachus anguineus,’’ (published 1937) of 190
quarto pages, 7 half-tone plates and 128 text-figures. In
shark anatomy this book, on one shark only, measures up
No. 794] BERTRAM GARNER SMITH 583
to J. F. Daniel’s ‘‘ Hlasmobranch Fishes’’ (3rd. ed., 1984,
octavo, 322 pp., 270 figs.).
But even this was equalled by the final article in the
Memorial Volume, ‘‘The Heterodontid Sharks: Their
Natural History and the Development of Heterodontus
japonicus, Based on Notes and Drawings by Bashford
Dean.’’—138 quarto pp., 7 lithographed plates (5 in
natural color) and 69 text-figs. This I (as editor) had
held for Smith and for the final article in the Memorial
Volume, and when (October 1, 1942) I handed him the
first copy from the binder, I said, ‘‘This is the high note
of the Volume, and also of your scientific writings.’’ But
little did I apprehend how true the latter statement was
to be.
Dr. Smith retired from his work in N. Y. University,
September 1, 1942, settled up his affairs in the Hast and
presently went to Albuquerque, N. M., where he bought
a house and settled down to adapt it and the grounds
(with his own hands) to make it a home. Things went
well until in the Spring of 1945 he began to have heart
attacks, to one of which he succumbed on July 30. Thus
passed a fine man, who made elaborate studies of the
natural history and embryology of one of the least known
American amphibians. Later he made similar additions
to our knowledge of the natural history, anatomy and
embryology of two archaic sharks. These notable mono-
graphs, the outcome of ability and persistent hard work,
are the monuments in American Zoology to Dr. Bertram
Garner Smith.
RELE
BASHFORD DEAN MEMORIAL VOLUME
EN NOUS, JellSisles
Edited By
EUGENE WILLIS GUDGER
ArtTIcLe VI
fae ANA OMY OF Mrik PRIELED SkAIK
CHLAMYDOSELACHUS ANGUINEUS Garman
By BERTRAM G. SMITH
Professor of Anatomy
New York University College of Medicine
New York City
NEW YORK
PUBLISHED BY ORDER OF THE TRUSTEES
Issued December 22, 1937
ARTICLE VI
EAN AO MYSOE SHES ERICEE DE SEU AK
CHLAMYDOSELACHUS ANGUINEUS Garman
By Bertram G. SmitH
CONTENTS
INR ODO CLIO Ni teeee eer er BPR mon ma An 2 asd) aprsits ata Ree oem Oe 335
EXKERINAT @HARACTERSIORNC@ lami dosclachtspmrime i ae eiaiel aie ae eee 336
GENERATHR OR MIOFATHED BODYS Eee Rae eLRE CaE Ri Pi eee 336
JPkars eal onsy (Ova Unsdss INA MO\OAMEKS putts odo laia'o o okra plarho Miajows uaa ale alte dia ola caida kn ole Grobe aeow a 338
Gin GOVERSEAND 1 OPERA CLES Hi seecter tay temnel on War aucn wi Mayan. cata iatentseretaweelray ne Weiac aR eee reactor ny ee 339
RINSWRATREDVANDIWINPATRED A © cue can ciaccuelient, ca lsseen cle cycseie Moin tedisiey ates selfs canes eat pe yee rene cee 340
PAE DOMINATAO RMER OPEC UE OLDS ieee cui este Ine SIP MoH CET tae ene sree 342
SGIATE SWAIN DIMER TET aaa tip Sv aay pene oe stat ser tame tye ty HET AAR haps aii 8 VeVNE Go NU isin Seg SAO 342
FIBER END OSKE IEE: © NRE ict ii erain ee er RONG Deh cyanea ies acy ciate Edis fete ee ea Ege 350
SRUETROES ORIG MYGOSELAGHU SH rita a enero rated eras aaron eineataleyer ota suse aenete equ ane co Seaeueu rel 350
TUNETEN RIA NEUE aU MT OE OSSe OTT Te Raat ant antes TES UG EAE Se enter 351
ST TEN ASCERUATS SRELETON rte eeee eer ee aE Ceara ener oee eee: 356
INGROGEORD Ania WiranarUNG (COMET, 5 soca dooknunaesboumoocosouooHadboe bas Or00se 364
FAPPENDICULARTO KELE TON See Oruean tricone eR Meco cele ear iv eae EASED acu eT 370
PECTORIATNEINS AND) GIRDLE Spare creator reo oP eer ISO: Ri eee 370
PEL VIGREINS VAN DISPEL VIS MEY Sar ECT Ry ere eRe ST RL AAT AST TTS ohs Conse le Tore rater pees 373
SHE) DOR SATEEN AC sy ere rece Nee Eden Sioe EES LEU HE PRN OORT Sve PIS orsloke Ace eee 377
SIS WAIN A TAR IN Rete ore Re Serre Ce ANIA AHR no ciety a Stout, i ee REN Rit aoa re 380
SISTERS CAUDAL VEINE Aaya ee oO ea En OE SOE ences ree 380
BIWET EIN AWTS UIE AIRMO VST Eien Otte gr rm netgear eh aie ey a pM les th ue Ae ale ae 381
BSH RENAE TAQMERIC UNL USCLES oie Vert yee cc) SESE SERN canna SFL peeing os eRe 381
aE MAKTATC NLU SCLES ME GAIT ae eer ETRE A Sehr aR ROAR ISAC ES toe 382
Thine APPEN DICULARSNAUSCLES 1 0-02 Fest r RCN eee edna betel TRAE nd Aare leur eae eer 394
Waly RANGEMOMTARIG IMIURCHEB, oop coc od boos secon boo oo OOD OOO GOS OOO UUDODOOOODSSE 396
DIGESTIVE SYSTEM AND ASSOCIATED ORGANS. ........-0- 0000 eevee ee eee eee ee 401
MISE ODI GES TIVE SRW BERS are oe Se See et es CoC ones oi Siiatarcas aie aes cee eee 401
SSE PILAR Y NX han tetera eee ICT aCe ETT ee I or roe EE ee 402
IESOPHAGUSVANDS @ARDIAG STOMACH AAR nee Ca eEe Cece eo eee errr 402
SHIP YE ORICAWESTIBULE Nee tthe ooh cE Oo Er OETA er: REC er 404
STSETEUPVLOR UB RON Ree ape Re pete Eg esi EME eee Oe oT aE EE RE Cro ere 405
Sng BURSAGENTIAN AS ace ETAT Ecos EEE EEC OL On CER ER One nee 406
SHE AVAL VULARMINTESTINE Series accra TT RP TESS ere eee arr rete rere 408
IREGTUMPANDIRECTAL GLAND A sys ore A TT ESC LEVC RS See A eet ar Peete Se eee 410
BISHES DIGESTIVE WUBEPASTAM WHOLE Matec etcetera eee Lrernctersreeariieterayrercrmets 411
AIDE ENLGI WERE Pie ttt Fam eke on 2a ly OPER na cinta hac eat Lane ls Ses tebe ee Neaach, center anes 412
“a Dy ech 1 BAGS TSH NGA ora carne eee cine lee oes Herat eh te aapits ner See ase ane a atian cst ecifemereucn Eran acy ete 413
OrcGaAns AssOCIATED WITH THE DIGESTIVE TRACT.........2 200 cc eee eee eee eee eee renee 415
“Ndr IER aXolie) Cle Wine dink Roden Aue Hp UTERO eH SOM Hobe ance COOL DeM iE renames ae oo ey nado 415
GIR a GACT ACTA STI Ae UN tec ACW Aye aT RP Meee ta Me see east an Ror ee chet ce 418
PEE VRGESPIRCATORYA ORGANS] He toe tires eM ag cin ee ope ya aioe tee ours mask 419
MIRETE YG IETS Rees Are ape DUG e > RE lu cent. SUM tiet PRA Stes mechucrey ncn cuisvRe cane epicien tacks toma vietoteioh seistate ope 420
SINETE NS PIRVA CLES aes cle raya chem ooo EUs Dar eaten Stas ata caspenhe a tenets den ce scurpee ge Reeae cere 423
BISFIE WIR O GENIAL HOY STE NTE te teyrie os aerate ey Siesta averu a iy Faces uO ctl rrr ge peat Eg 431
WROGENELATIOYSTENUOELEHE PEE NCATE nine neta rene te etter neon etre tric Rea Ren tore 431
WROGENTTAT] SIN USHINETHEIREM ATE Ane nn Een eran ernin eerie tiene ceeieeeeieiires 431
ORGANS OFIEXCRETIONINITHRI FEMALE SEER een inte merce eee eccioniiracecn tanec 434
Grnrrari OrGANs|OR THE ;REMATE BREE Eee erecta eerie ieee eeeiacreiister 444
URGE STEN Shenae Ge Gis IMMUNO, coco ooo noobs ooo DUD oOo DOD CON CU UNDDOO DAHL ODOOUEE 450
EXCRETORYSANDI INTERNAL GENITAL) ORGANS EE eiciicisteisicinicinicie ciate ee ciiaieteeiietiiicicrinieieieieieielsiseiste 450
INATROPTERY GIAVOR CUASPBRS 35 c5:c1s cre pT TSE NOS PY TN Ten eT a creyststsictensiee esevanersierapelcror 451
ARHERAIBDOMINATY E ORES tic 5cieun Seer. cee SO TU OLIILIE CIs Ci AIMS Scene nine) sqstsudityans 453
HES SENSER ORGANS See eee
BSTEINIEMBRIAN@ USHIGABYRINTHt liu. bcerrresctrek Meret Mate (ay) Rol m eae PVCS eit Se URE
AIRTIER SENSOR VA CANAT OVSTE Mie ira tt, © hee teal ae ehs oe Retin coarse Ue ene ae
[DISC USSTO Neeser eee eh tts ee Bs on ane DUNS OA) he 8 Sette ks Bee em See eee ae :
| BUTSHETLO GRATE Ge aie Sea rc te te tm PA See aR ROGER mM NTR Oat RA a cael Al i
334
THE ANATOMY OF THE FRILLED SHARK
CHLAMYDOSELACHUS ANGUINEUS Garman
By Bertram G. SMITH
Professor of Anatomy
New York University College of Medicine
INTRODUCTION
Interest in Chlamydoselachus centers around the problem of its affinities. It has been
said (Garman, 1884.1, .2) to have “‘a certain embryonic look.” It has been called a living
fossil. It has been designated (Garman, 1884.3, .4; Gill, 1884.1,.2) the oldest living type
of vertebrate. More conservatively, Woodward (1921, p. 37) regards Chlamydoselachus
as one of the most primitive of the true Selachii. On the other hand, a study of the
external characters alone (Gudger and Smith, 1933) is sufficient to indicate that Chlamy-
doselachus possesses many structural adaptations of a very special nature. In the present
article I have endeavored to distinguish those features that represent a high degree of
differentiation, from others that link Chlamydoselachus with the most primitive fishes.
Since the publication of Garman’s (1885.2) description of a partly eviscerated speci-
men with a slightly mutilated tail, there has been no comprehensive account of the
anatomy of Chlamydoselachus; but there have been many investigations dealing with
particular organs or parts of the body of this rare fish. Some of these contributions were
published in such form as to be readily accessible, but much information concerning the
structure of Chlamydoselachus lies buried under titles of a somewhat general nature.
In bringing together a digest of all these records I have endeavored to supplement them,
wherever it seemed desirable and practicable, by original observations on all the ma-
terial available.
This material includes three large female specimens (lengths 1350 mm., 1485 mm.
and 1550 mm. respectively) brought from Japan by Dr. Bashford Dean, and now in the
collections of the American Museum of Natural History; and a fourth large female
specimen (1398 mm. long) kindly lent by Dr. E. Grace White. The first three specimens
had been preserved in formalin and alcohol for about thirty years. The fourth shark
had been preserved in formalin, then alcohol, for an unknown period. In all the specimens
the viscera were in a more or less unsatisfactory condition for study, and from the fourth
specimen the digestive organs had been entirely removed. Nevertheless, a careful exami-
EDITOR’S NOTE:—The first study of the anatomy of Chlamydoselachus was made by Samuel Garman at the Museum of Com-
parative Zoology, Cambridge, Mass., on the first specimen ever brought to America (1884). Garman’s monograph was published in
1885 and is referred to herein as 1885.2 The original drawings and the woodcuts made from these have fortunately been preserved
in Cambridge. They have been most kindly sent to me by Dr. Thomas Barbour, Director of the Museum of Comparative Zoology.
Many of the woodcuts have become warped and split by drying during the past half century, but it is a great satisfaction to be
able to use three of them (Text-figures 94, and 101a-s) in this paper, and to have new cuts made from certain of the original draw-
ings—those representing the brain, which are reproduced here as Plate VI.
335
336 Bashford Dean Memorial Volume
nation of this material has enabled me to fill in some of the most important gaps in the
hitherto available knowledge of the gross structure of Chlamydoselachus. Our knowledge
of this interesting fish is still incomplete, and one purpose of the present article is to
direct attention to the opportunities for investigation that still exist for one who is able
to secure favorable material.
Since the anatomy of the lower vertebrates is of interest chiefly from the comparative
point of view, I have endeavored, within the limits imposed by practical considerations,
to point out some of the resemblances and differences between Chlamydoselachus and
other primitive sharks—particularly its nearest relatives, the Notidanidae. Fortunately
for my purpose one of these, Heptanchus maculatus, forms the basis of Daniel's (1934)
masterly treatise on the anatomy of the elasmobranch fishes—a volume which I have
found very helpful.
For those who view this and similar undertakings from afar, it may be permissible
to state that only anatomists and embryologists realize how much the study of elasmo-
branchs has contributed to our understanding of the present structure and past history
of the human body.
EXTERNAL CHARACTERS OF CHLAMYDOSELACHUS
Since the external characters of the frilled shark have been described in detail by
Gudger and Smith (1933), only a few of these features which are of particular significance
for comparative anatomy need be considered here.
GENERAL FORM OF THE BODY
As compared with other sharks, Chlamydoselachus (Text-figure 1) is very slender.
Therefore it is pertinent to inquire what an elongate form of body means in the evolution
ary history of a group of vertebrates. In general, the most primitive members of any
large and divergent group are only moderately elongate, while a high degree of speciali-
Text-figure 1.
Chlamydoselachus anguineus Garman, adult female, 1473 mm. long.
After Dean, 1895, Fig. 92; redrawn from Gunther, 1887, Pl. LXIV.
The Anatomy of Chlamydoselachus 337
zation may affect the body form in either of
two ways: the body may become short and
broad, as in skates, frogs and turtles; or it
may become very slender, as in eels, coecil-
ians and snakes. A consideration of the
evidence upon which this generalization is
based would take us too far afield, but it is
a principle that appears to be accepted by
most comparative anatomists.
In the case of Chlamydoselachus, the
elongation of the body has proceeded far
enough to remove it from the category of Sa
primitive characters. It serves, perhaps, as XY ih SN
an adaptation to life on a rough sea bottom, Af ¥ YW _
where the animal is obliged, occasionally, to ;
swim or crawl through crevices. In such Text-figure 2.
situations, Chlamydoselachus may lie in hid’ Front view of the widely-distended mouth of
ing, or may even stalk its prey, then strike specimen of Chlamydoselachus collected in
: Japanese waters by Dr. Bashford Dean and
suddenly as doesa snake. But there is another aiosaaicel (9 Caltmibn Unniarster,
advantage to be gained from an elongate After Gudger and Smith, 1933, Fig. 3, pl. X.
form of body. It may be observed that the
ectoparasitic cyclostomes have bodies that are very slender, and that Echeneis, the
sucking fish, also is slender-bodied. These are creatures that fasten on to fishes larger than
themselves and are towed along by the host. Owing to the slenderness of their bodies
they are not readily shaken off. Because of the large mouth and the prehensile teeth
(Text-figure 2), it has been surmised (Gudger and Smith, 1933) that Chlamydoselachus
seizes and swallows living prey nearly as large as itself. The swallowing of a large fish
struggling to escape is presumably not an easy matter, and were Chlamydoselachus a form
that offered much resistance to being dragged through the water, it might not be able to
maintain its initial hold.
Text-figure 3.
Heptanchus (Heptabranchias) maculatus, adult female.
NWN, nares; SP, spiracle.
After Dean, 1895, Fig. 93.
338 Bashford Dean Memorial Volume
More than in most sharks, the head of Chlamydoselachus, though not its body, is
decidedly flattened in a dorsoventral direction when the jaws are closed. This, together
with the fact that the creature is usually taken at great depths, suggests that the frilled
shark is, at least partly, a bottom-dwelling form. We need not, however, conclude that
the flattening of the head tends to remove Chlamydoselachus from the category of archaic
fishes. ‘For various reasons it seems likely that the primitive chordates were not swift-
swimming, pelagic types but partly depressed, partly bottom-living forms” (Gregory,
1933, p. 101).
Among living sharks the notidanid Heptanchus maculatus (Text-figure 3), though
stouter-bodied than Chlamydoselachus, presents the greatest similarity in general form,
position and shape of the fins, and in the shape of the tail. Throughout the present
article I have made many comparisons between Chlamydoselachus and Heptanchus. Dean
(1895) stated that “Heptanchus, of all living sharks, inherits possibly to the greatest
extent the features of its remote ancestors.” This is doubtless still a fair generalization
when one considers only the external characters, but in many, perhaps most, of the
internal structures described in the present article, Chlamydoselachus is less specialized
than Heptanchus.
POSITION OF THE MOUTH
In Chlamydoselachus the mouth is sub-terminal (Text-figure 4, after Garman), but
it approaches a terminal position to a degree found in no other shark, so far as I know,
save only Rhineodon, the whale-shark. Sharks are preeminently surface-feeding forms,
but the mouth is usually ventral. In skates and rays, which are bottom-feeding fishes, the
mouth is decidedly ventral. In teleosts, with the exception of a few bottom-feeding
forms, the mouth is terminal or subterminal. Thus in fishes the position of the mouth is
decidedly variable. In linking the great groups of fishes, to assign phylogenetic value to
such a character is hazardous. One cannot fail to note the resemblance, in the position of
the mouth, between Chlamydoselachus and the teleosts, but their real relationship must
be decided on the basis of more stable characters. Nevertheless, it may be pertinent to
inquire, what is the primitive position of the mouth in the vertebrates?
Since in vertebrate embryos the mouth is ventrally situated, one might infer that
this position is primitive for vertebrates. This inference is not supported by all the
facts of development. The ventral position of the mouth of a vertebrate embryo is due,
in part to a precocious enlargement of the anterior end of the brain, in part to the cephalic
and cervical flexures which, in later development, tend to straighten out. If we consider
only adult structures and accept the time-honored theory that the jaws represent a modi-
fied gill-arch, then the mouth is formed on the morphologically anterior side of this gill-
arch. In its primitive position the mouth would naturally open forward, though situated
at a lower level than the cranium and to this extent not fully terminal. The vertebrate
mouth is, primarily, anteroventral or subterminal.
The Anatomy of Chlamydoselachus 339
From its primitive position, the mouth may be displaced either ventrally or terminal
ly. In elasmobranchs it is usually displaced ventrally by the thickening and forward
elongation of the cranium to forma rostrum. In other words, when the cranium becomes
extended anteriorly, the mouth of necessity becomes ventral. This may occur regardless
of the size of the mouth. In the basking shark, Cetorhinus, the mouth is very large but is
nevertheless ventral because of the elongate snout. In the sawfishes the prolongation of
the rostrum is carried to an extreme that makes the mouth decidedly ventral. In teleosts
the mouth tends more often to become terminal, though in some forms, as in the fresh-
water suckers, it is brought into a ventral position by an extensive development of the
related soft parts.
I conclude that, in connection with its enormous enlargement, the mouth of Chlamy-
doselachus has departed only slightly from the primitive orientation, and that this de-
parture has been in the direction of a more nearly terminal position. The anatomical
basis for this condition is described more fully in the section on the skull. The position
of the mouth is decidedly more primitive in Chlamydoselachus than it is in most elasmo-
branchs; it shows a closer parallel with the condition usually found in teleosts. But
there is substantial evidence, which cannot be considered here, indicating that the line
of cleavage between elasmobranchs and teleostomes extends back to forms more general-
ized than any living fish.
GILL-COVERS AND SPIRACLES
The presence, in Chlamydoselachus, of a sixth pair of gill-slits has usually been
accounted a primitive character of considerable phylogenetic importance, linking Chlamy-
doselachus with the notidanids. But Pliotrema, a sawfish, has six pairs of gill slits (Regan,
1906.1), differing in this respect from other sawfishes. While there is abundant ground for
the conviction that Chlamydoselachus is related to the notidanids, one must not lean too
heavily on the evidence afforded by the number of gill-slits. “In the existing elasmo-
branchs the normal number of gills is five and it may well be suspected that the six or
seven gill-slits of the notidanids and the six of Pliotrema represent a secondary increase
in number” (Gregory, 1933, p. 424).
In Chlamydoselachus, the unusually well developed first pair of gill-covers (Text-
figure 4), continuous as the gular fold across the mid-ventral line, simulates an operculum
such as is found in bony fishes. Garman (1884.2) suggested that this operculum-like
fold or collar of Chlamydoselachus is a character indicating that the frilled shark lies near
Text-figure 4.
A side view of the head of Chlamydoselachus to
show the position of the mouth, the length of the
lower jaw, the position of the nostril and of the
eye, and the position and form of the gill-covers;
about one-fourth natural size.
After Garman, 1885.2, pl. I.
340 Bashford Dean Memorial Volume
the primitive stock from which elasmobranchs and teleostomes diverged. On this point,
Dr. W. K. Gregory, in a personal communication, commented as follows: ‘“The idea that
Chlamydoselachus stands nearer to the true fishes than do the sharks proper, is without
a vestige of real evidence in its favor and with a mountain of evidence against it.”
In Chlamydoselachus the external openings of the spiracles (Text-figures 70, p. 396;
and 124, p. 489) are very small. In the notidanids the spiracles are said to be small.
In some sharks that certainly bear no close resemblance to Chlamydoselachus, spiracles
are absent altogether. In skates and rays, which are bottom-dwelling forms, the spiracles
are proportionally large. It has been inferred that spiracles were developed in connection
with a sea-bottom habitat; but this is true only of the valvular apparatus which, in skates
and rays, enables the spiracle to function for the intake of water when the mouth is buried
in sand or mud. In Squatina, a bottom-dwelling shark, the spiracles sometimes admit
water to the oropharyngeal cavity. But sharks are characteristically free-swimming
forms in which the spiracles, if present, serve merely for the exit of water from the pharyn-
geal cavity, thereby retaining their primitive function as gill-slits. This is the function
of the spiracles even in Chlamydoselachus, as will appear from the description of the
spiracular canal (p. 423) in the section on the respiratory organs.
The small size of the external spiracular openings of Chlamydoselachus affords
evidence that the spiracles are in a vestigial, not an incipient condition. Spiracles have
not arisen de novo; they represent merely a modification, sometimes accompanied by
a change in function, of a primitive pair of gill-slits situated between the mandibular and
the hyoid arches. In the process of transformation of this primitive anterior pair of
gill-slits into spiracles, the ventral portions of the openings close, while the dorsal portions
persist—as is shown in Text-figure 62, p. 388. The internal aperture is much larger than
the external. If one opens the mouth of any shark possessing spiracles, he will find a pair
of large internal spiracular openings resembling gill-slits, in exact serial relation with the
dorsal portions of the gill-slits. In Chlamydoselachus, whose external spiracular opening
is a slit only 2 or 3 mm. long (Text-figures 70, p. 396; and 124, p. 489), the internal spiracu-
lar orifice is an elliptical aperture more than 20 mm. long and wide enough to admit easily
the blunt end of a pencil. As in many other selachians, the spiracles of Chlamydoselachus
possess vestigial gills, called pseudobranchs.
FINS, PAIRED AND UNPAIRED
The bunching of the pelvic, ventral and dorsal fins near the caudal (Text-figure 1)
gives color to Garman’s view (1884.1, .2) that these fins provide the creature with a ful-
crum from which to strike. This arrangement of the fins is a very special feature. The
pelvic fins, the anal fin and the ventral lobe of the caudal fin are sufficiently large to in-
dicate that Chlamydoselachus is not closely confined to the sea bottom. The shape of the
tail is much like that of Heptanchus (Text-figure 3).
The weakness of the fins of Chlamydoselachus is due not only to the softness and
fineness of the dermal fin rays, which are exoskeletal structures, but also to the rudimen-
The Anatomy of Chlamydoselachus 341
tary character of the cartilaginous rods, particularly the radials, that stiffen the basal
portions of the fins. These rods belong to the endoskeleton and will be further con-
sidered in their proper place. In all the fins there is a wide expanse supported only by
fine dermal fin rays. From the viewpoint of adaptation to environment, one may say
that softness and flexibility of the fins is an advantage to a fish that must make its way
through crevices in a rough sea bottom. In such a situation, stiff fins might be a decided
impediment. Evidently Chlamydoselachus is not a rapid swimmer, since it must depend
for locomotion partly upon serpentine movements of a slender body.
WKH Een
RAAqauogs
Text-figure 5.
Restoration of the Devonian shark, Cladoselache. Its fins were supported by simple
parallel rods of cartilage extending nearly to the margin.
After Dean, 1909, Fig. 41.
In the earliest fossil remains of sharks that appear to have left modern descendants,
the parallel rods of cartilage (radials) that support each fin extend almost to its margin,
so that the entire fin must have been fairly rigid (e. g., as in Cladoselache, Text-figure 5).
In living sharks there has been a reduction and modification of the radials and a correspond-
ingly greater dependence on dermal rays for stiffening the fins. In Chlamydoselachus
the reduction of the radials has proceeded to an unusual degree but without a compen-
sating development of the dermal rays.
The shortness and breadth of base of the fins of Chlamydoselachus bring to mind the
fin-fold theory (Thacher, 1877; Balfour, 1878; Mivart, 1879) for the origin of the fins of
fishes; but fins that are broad and short are found in some of the most highly specialized
sharks and more notably in the skates and rays. So this form of fin is not necessarily
primitive. In Chlamydoselachus, the shortness and breadth of the fins are in strict harmo-
ny with the marked elongation of the body which we consider a departure from the norm
for primitive fishes.
In discussing a series of elasmobranchs (Cladoselache, typically Devonian; Pleuracan-
thus, typically Permo-Carboniferous; Hybodus, typically Jurassic; and Chlamydosela-
342 Bashford Dean Memorial Volume
chus, now existing but exemplifying the Cretaceous and Tertiary type) selected to
illustrate the types prevailing in successive periods of time, Woodward (1921) says:
“Very soon the remnants of lateral fin folds, which must have acted merely as two pairs
of balancers in these fishes [the earliest known fossil elasmobranchs] concentrated into
paddles, and these again passed into stout-based fins adapted for swimming.” It is not
explicitly stated, by the author quoted, that he regards this succession of types of paired
fins as a phylogenetic series, but one may infer that he considers the breadth of base of
the paired fins of Hybodus and Chlamydoselachus as something secondarily acquired.
It is known that Dean was an ardent advocate of the fin-fold theory for which he
(1894 and 1895) obtained interesting evidence in the case of the fossil Cladoselache
(Text-figure 5). The question of the origin of paired fins was one of the problems Dean
had in mind while he was searching in Japanese waters for embryos of Chlamydoselachus,
Cestracion (Heterodontus) and other primitive fishes. Subsequently, Dean’s material
was studied by Osburn (1906 and 1907) who defended the fin-fold theory against
the attacks of those who favored the opposing gill-arch theory originally proposed by
Gegenbaur (1865).
ABDOMINAL OR TROPEIC FOLDS
The abdominal or tropeic folds are a pair of slender longitudinal thickenings of the
ventral abdominal wall, situated close to the median line and separated by an external
groove. They are figured and comprehensively described by Gudger and Smith (1933, pp.
283-284, Text-fig. 12), and are shown in transverse section in various figures inserted
in my chapter on the muscular system (p. 381).
No satisfactory explanation has ever been advanced to account for the presence of
the tropeic folds, which are structures peculiar to Chlamydoselachus. Concerning them
Garman (1885.2, p. 3) wrote: “From their position, shape and extent, it is evident that
the folds will furnish support to one of the theories regarding the origin of paired fins.”
I agree with Braus (1898) that “Der Kiel des Chlamydoselachus hat zur Genese der
paarigen Gliedmassen nicht die geringste Beziehung.” In my section on the muscular
system there is given a fairly satisfactory explanation (illustrated by Text-figure 58, p. 386)
as to the manner of embryonic development, but this does not answer the question as to
the fitness of these peculiar structures for the needs of Chlamydoselachus in its particular
environment. One can infer from their form and position that they may have some slight
utility in locomotion similar to that afforded by the keel of a ship: but in some specimens
they are too small to be of any appreciable use in this way.
SCALES AND TEETH
The variations in the form of the placoid scales or dermal denticles of Chlamy-
doselachus on different parts of the body, the form of the teeth, and the arrangement of
the teeth in rows have been described by Garman (1885.2), Rdse (1895), and by Gudger
The Anatomy of Chlamydoselachus 343
and Smith (1933). We are here concerned chiefly with the structural and developmental
relations between scales and teeth. The latter are not ordinarily considered as external
structures, but are discussed here because of their morphological relationship to scales.
Some typical scales of Chlamydoselachus are shown in Text-figure 6. Each scale is,
essentially, a hollow cone with ridges extending from the base to the apex. It is composed
of dentine covered with a thin layer of enamel. In addition to the single prominent
spine there are sometimes, as shown in Text-figure 6a, slight elevations near the margin
of the base, formed by intersecting ridges. These elevations might easily develop into
Text-figure 6.
Three different views of a placoid scale or dermal denticle (x 130) from a 340-mm. embryo of Chlamy-
doselachus: A, scale from the flank, viewed from above; B, lateral view of a scale from the region of
the tail; C, scale from the region of the tail, seen from beneath.
After Rose, 1895, Abb. 1, 2, 3.
accessory spines. Of the atypical scales, those forming the ‘‘armature” on the anterior
edge of the dorsal fin (Garman, 1885.2, p. 7; Gudger and Smith, 1933, p. 204) are interest-
ing because, in form and arrangement, they resemble the “‘fulcral scales” of the Actin-
opterygit. The latter are described by Goodrich (1909, p. 304), and are said to be quite
peculiar to this group.
A typical tooth, viewed from three aspects, is represented in Text-figure 7. It
has three sharp, slender, curved cusps, and two rudimentary cusps or denticles. It is
attached to the jaw in such fashion that the denticles project inward toward the mouth
cavity. The broad base of the tooth is prolonged posteriorly (toward the interior of the
mouth) and is forked so as to interlock with a paired excavation in the base of the suc-
ceeding tooth. In the illustrations the prongs of the base might readily be mistaken for
cusps, but in the actual specimens the appearance is very different since the base is com’
posed entirely of dentine while the cusps are covered with shiny white enamel.
344 Bashford Dean Memorial Volume
Text-figure 7.
Three different views of a tooth of Chlamydoselachus, six times natural size:
A, seen from above; B, from the side; C, from beneath.
After Garman, 1885.2, Figs. 1, 3 and 4, pl. VI.
The essential similarity of the internal structure in scales and teeth of sharks is
evident from a comparison of Textfigure 8 with Text-figure 9. Each has the form of
a hollow cone, slightly recurved at the apex. Each is composed of dentine (D., D.2)
overlaid with enamel (e., S.). The dentine is traversed by canals (d. c.) radiating from the
pulp cavity (p. c. and P.).
Both scales and teeth are exoskeletal structures. Evidently teeth, which are the
more complex, have developed from the same materials and in the same manner as scales.
It would, perhaps, be a trifle crude to say that teeth are developed from scales, but it
seems entirely proper to say that teeth are homologous with scales. This has long been
admitted, but in Chlamydoselachus we have material exceptionally favorable for revealing
the precise manner in which teeth correspond to scales. Superficially, the chief difference
Text-figure 8. Text-figure 9.
Sagittal sections showing similarity of structure between scales and teeth of sharks.
Text-figure 8. Section showing finer structure of a placoid scale of Scymnus lichia.
c.c. central canal; d.c., dentinal canal; e., enamel; p.c., pulp cavity.
After Daniel, 1934, Fig. 35; redrawn from Hertwig, 1874, Fig. 2, Taf. XII.
Textfigure 9. Section of a single-cusped tooth (x 75) from the lower jaw of a
340mm. embryo of Chlamydoselachus.
D., dentine; D.2, strongly calcified dentine; P., pulp cavity; S., enamel; So., base,
After Rose, 1895, Abb. 9,
The Anatomy of Chlamydoselachus 345
between a scale and a tooth in Chlamydoselachus is that the scale has but one projection
large enough to be called a spine, while the tooth usually has three large spines or cusps,
and two rudimentary cusps. The question arises: does a single scale correspond to an
entire tooth, or does a tooth develop as an aggregate of several scale-like rudiments?
Near the angles of the mouth of Chlamydoselachus, teeth sometimes grade into
scales. In the four large specimens studied by Gudger and Smith (1933), the teeth of the
last rows, as these approach the angles of the jaws, become very small, irregular and
rudimentary until finally it is with great difficulty, even with the aid of a strong lens,
that rows of teeth can be distinguished from groups of undoubted scales like those shown
in Text-figure 10. The teeth are not comparable to individual scales, but each cusp
Text-figure 10.
Placoid scales or dermal denticles
(x 5) from the angle of the mouth of
Chlamydoselachus. Each scale re-
sembles a single cusp of the rudimen-
tary three-cusped teeth occurring in
this region.
After Garman, 1885.2, Fig. 12, pl. VI.
resembles a scale, and the scales are sometimes arranged in columns of threes in series
with the rows of teeth. In two specimens the border line between teeth and scales
could be distinguished with considerable certainty, but in the other two specimens there
was room for doubt. On the other hand, Garman (1885.2, p. 5) says of his single adult
specimen: “the change from teeth with broad base, three cusps, and two buttons [rudi-
mentary cusps] is sudden and decided; i.e., they do not grade into each other. A strong
lens, however, is necessary to distinguish them, since in the hinder row each cusp looks
much like a single scale.” The last statement, together with the observations of Gudger
and Smith, suggests a multiple origin for each tooth.
The development of a placoid scale has not been studied in Chlamydoselachus; but
in the leopard shark, Triakis semifasciatus, a scale develops from a single primordium
(Daniel, 1934, p. 26 and Fig. 29). It is of interest to inquire whether the multicusped
teeth of Chlamydoselachus develop in the same manner.
The teeth of a 340 mm. embryo of Chlamydoselachus have been studied by Rose
(1895). In this embryo, none of the teeth (Text-figure 11) had attained its final form, but
some in the middle of each row were like those of the adult except that they lacked the
two very small cusps. The innermost teeth of each row were represented, individually,
by three distinct cusps not yet united at their bases; apparently each cusp had developed
from a separate primordium. The evidence certainly indicates that, at the inner end of
346 Bashford Dean Memorial Volume
each row, teeth were being formed by the
union of simple denticles homologous with
placoid scales. At the outer ends of the
rows, the teeth were small and rudimentary;
each tooth had from one to three cusps.
Those with a single cusp bore a strong resem-
blance to placoid scales. In the teeth with
two or three cusps, the cusps were so closely
fused at their bases that the enamel was con-
tinuous from one cusp to another. According
to Rose, these teeth represent a stage transi-
tional to the adult teeth of many teleosts.
Possibly these teeth were anomalous, since in
my four large specimens the outer teeth are
only slightly different from those at the middle
of each row: all have three cusps well devel-
oped and well separated. Rose thinks that all
the two- and three-cusped teeth of his embryo
developed through the fusion of simple cusps.
Textfigure 11. On one side of the upper jaw of his em-
Teeth of the lower jaw (x 5) of a 340-mm. embryo bryo, Rose found the first two teeth of the
of Chlamydoselachus, in their natural positions. 5 5 Re,
eat SRO. IS third row united at their bases, but delimited
by a deep groove (Text-figure 12 herein). One
of these teeth has but one cusp, the other has two cusps. Rose claims that this
anomaly has a phylogenetic significance, since it indicates the manner in which a jawbone
might arise through the fusion of teeth at their bases. Further, Rose asserts that the
three- and especially the five-cusped teeth of an adult Chlamydoselachus furnish an
excellent transition between a single-cusped shark tooth and the toothplates of an adult
Siren, likewise of all urodele embryos. Also, he finds in his Chlamydoselachus embryo
all possible forms intermediate between a simple placoid scale and a three-cusped tooth.
The single-cusped tooth shown at the left in Text-figure 12 differs very little from a simple
scale and is smaller than some of the scales found on the external surface of the body.
Rése calls attention to the fact that in Chlamydoselachus the dentine (illustrated by his
Fig. 10) develops in fundamentally the same way as in mammals.
Text-figure 12.
The first two teeth (x 45) of the third
row of the upper jaw of a 340mm.
embryo of Chlamydoselachus. These
teeth are united at their bases.
After Rése, 1895, Abb. 6.
The Anatomy of Chlamydoselachus
Text-figure 13.
Placoid scales from two species of the Devonian shark Cladoselache.
A—Scales (x 25) from various parts of the body of C. fyleri. From a specimen in
the American Museum.
B—Trifid scale (x 20) from near margin of mouth of C. fyleri. From a specimen in
the American Museum.
C—Larger scales (x 10) of Cladoselache (probably clarki). From a specimen in the
British Museum.
After Dean, 1909, Figs. 1, 2, 3.
347
In Chlamydoselachus and in Heptanchus (Daniel, 1934, Fig. 27) the structure of the
scales is simple and conforms to the same fundamental plan, though in both fishes the
form of the scales varies considerably on different parts of the body. One should not
attribute much phylogenetic importance to differences in the form of the scales of elas-
mobranchs. Some of the most specialized elasmobranchs (e.g., Raja) have simple scales,
while the fossil Cladoselache, one of the most primitive sharks, has scales of various
forms ranging from those only slightly indented or subdivided (Text-figures 13a and s)
to those indented to such a degree that their exposed surfaces bristle with cusp-like
points or ridges (Text-figure 13c.) In Cladoselache as in modern sharks, the scales vary
in size and shape in different regions of the body (Dean, 1909, p. 214).
The teeth of Chlamydoselachus are
barb-like, prehensile. In Heptanchus
(Text-figure 14) the teeth are not alike on
upper and lower jaws. The upper teeth
seem adapted mainly for holding, the lower
ones for cutting. The decided differences
between the teeth of Chlamydoselachus
and Heptanchus—forms which, in many
important respects, seem closely related—
serve to weaken one’s faith in the validity
Text-figure 14.
Dentition of Heptanchus (Notidanus) indicus.
a, teeth in function; b, teeth in reserve; u and I, upper and
lower single teeth (natural size).
From Goodrich, 1909, after Gunther,
348 Bashford Dean Memorial Volume
Textfigure 15. Text-figure 16.
Teeth of two fossil Chlamydoselachids from the Tertiary.
Text-figure 15. Fossil teeth of Chlamydoselachus lawleyi from the Pliocene of Orciano,
Tuscany, Italy. Note the lack of rudimentary cusps.
1 and 1b, teeth viewed from above; 1a, from below; Ic, from the side (1b, natural size; all others x 2).
After Lawley, 1876, Figs. 1 to Ic, pl. I.
Text-figure 16. A fossil tooth (A, natural size; B, x 2) of Chlamydoselachus tobleri from
Trinidad, British West Indies. Note presence of rudimentary cusps.
After Leriche, 1929.
of phylogenetic deductions based on a comparison of present-day fishes with fossil forms
that are known only by their teeth.
In the fossil Chlamydoselachus lawleyi (Lawley, 1876), which is known only by
its teeth (Text-figure 15), the resemblance to the teeth of C. anguineus is very close.
Apart from their smaller size, the teeth of C. lawleyi differ from those of C. anguineus
only in that they lack the pair of very small cusps. In C. tobleri, which is known only
from a single fossil tooth (Leriche, 1929), the small cusps are present, but in some other
respects the tooth (Text-figure 16) is so different that one may regard the inclusion of
this form in the genus Chlamydoselachus as merely tentative.
Text-figure 17. Text-figure 18. Text-figure 19. Text-figure 20.
Teeth somewhat resembling those of Chlamydoselachus anguineus, from various fossil sharks.
Textfigure 17. Tooth (x 5) of Cladoselache fyleri from the Devonian.
After Dean, 1909, Fig. 5.
Text-figure 18. Tooth of Cladodus acutus from the upper Devonian.
After Agassiz, 1843.
Textfigure 19. Tooth of Ctenacanthus clarki from the Carboniferous.
After Dean, 1909, Fig. 42.
Textfigure 20. Tooth of Hybodus reticulatus from the lower Jurassic.
After Zittel, 1923, Fig. 93.
The Anatomy of Chlamydoselachus 349
Among fossil forms assigned to other genera, teeth more or less resembling those
of Chlamydoselachus anguineus are found in Cladoselache (Text-figure 17), in Cladodus
(Text-figure 18), in Ctenacanthus (Text-figure 19), and in Hybodus (Text-figure 20). In
each of these fossil sharks the teeth vary in form, but those represented in the figures
may be regarded as typical. In all these teeth the cusps are conical, and the central
cusp is by far the most prominent. In Hybodus the lateral cusps (3 or 4 on each side)
become smaller in proportion to their distance from the central cusp. In Cladodus,
Ctenacanthus and Cladoselache there are two cusps on each side of the central cusp, and
the marginal cusps are larger than the intermediate cusps. In Cladoselache the inter-
mediate cusps are very small, as in the frilled shark. In Hybodus and in Cladodus most
of the cusps are recurved at the tip. In Ctenacanthus and in Cladoselache the cusps are
more slender and appear practically straight, though Dean (1909) states that in Clado-
selache clarki there is a slight sigmoid flexure of the cusps. Of the four forms considered,
Cladoselache possesses the sharpest cusps. In this, as in many other respects, the teeth
of Cladoselache most nearly resemble those of the frilled shark, but in this connection
I quote the following from Dean, 1909, p. 253:
When teeth of the type of Cladodus were discovered in different horizons from the
Devonian well into the Mesozoic, it was naturally concluded that the sharks themselves would
be found to correspond closely—to belong if not to the same genus at least to the same family.
When, however, associated remains of the earlier forms were discovered, it became clear
that these sharks were by no means closely allied. Instead of being proven to be cestracionts,
one type of “Cladodus” (Cladoselache kepleri, C. fyleri; Upper Devonian), was found to be
spineless, and quite different in essential structures from the modern cestraciont: another
type of “Cladodus,” Symmorium Cope (Coal Measures), was then shown to be unlike both
Cestracion and Cladoselache; and still another, ““Cladodus” neilsoni, was demonstrated by
Traquair to be quite different in fin characters from all the rest. And now a fourth cladodont,
Ctenacanthus, is found notably discrepant. It is, then, only the mesozoic group of “clado-
donts” typified by Hybodus which remains faithful to our preconceived notions as to what
kind of a shark a cladodont tooth should predicate. The fact of the matter is that the clado-
dont type of tooth is as ancient as it has been useful in the subclass Elasmobranchii, and that
it has appeared in many different lines, either as an heirloom from primitive sharks, or, less
probably, as an independent acquisition. Certain it is that it appears with little variation
in as many as seven families of sharks, and in at least three distinct orders.
When teeth are highly differentiated, resemblances amounting almost to identity
(as between Chlamydoselachus anguineus and C. lawleyi) are probably significant. On
the other hand, among living fishes we find instances where members of the same family
have widely different teeth. On a priori grounds it seems likely that, where cusps are
numerous and close together, development may proceed by the elimination of some of the
cusps in order that the others may be better nourished; or, putting the matter in another
way, some cusps may develop at the expense of the others. It seems probable that, in
the long lapse of time, teeth like those of Chlamydoselachus anguineus could have evolved
out of rather irregular and rudimentary structures, like the teeth of Hybodus reticulatus
350 Bashford Dean Memorial Volume
(Text-figure 20), quite as readily as from teeth like those of Ctenacanthus clarki (Text-
figure 19), Cladodus acutus Ag. (Text-figure 18) and Cladoselache fyleri (Text-figure 17),
which they more nearly resemble.
THE ENDOSKELETON
The most comprehensive studies of the endoskeleton of Chlamydoselachus are those
of Garman (1885.2), Deinega (1909 and 1923), and Goodey (1910.1). In addition, Gunther
(1887) described the skeleton of the claspers; Braus (1902) that of the paired fins; Fur-
bringer (1903) and Garman (1913) the visceral skeleton; while Allis (1923), using material
supplied by Dr. Bashford Dean, described the skull. Deinega’s first (1909) paper is
in Russian, but his original figures are reproduced in his later (1923) paper which
is in German.
As in selachians generally, the endoskeleton (excepting the notochord) of Chlamy-
doselachus is composed entirely of cartilage. In most elasmobranchs the cartilage is in
many places hardened by deposits of calcareous material without, however, assuming the
histological character of true bone. In Chlamydoselachus, it appears that such calcifi-
cation is very limited in extent. Thus Garman (1885.2) writes that the cartilage of the
skull is soft except in the parachordal region where it is hard and granular. Allis (1923)
says of the skull of Chlamydoselachus: ‘“The entire posteroventral region of the chon-
drocranium is extensively calcified in all my specimens, my observations thus differing
from Goodey’s” (1910.1, p. 553). Goodey does mention (p. 543) a calcification of the
floor of the cranium in the region of its junction with the vertebral column, and elsewhere
in the same article he describes local calcifications forming the rudimentary centra of the
vertebrae, but he emphasizes (p. 553) “the small amount of calcification appearing in the
skeleton at all.”
In the softness of its cartilaginous endoskeleton, Chlamydoselachus agrees with
Heptanchus which, according to Daniel (1934), has cartilage of the clear hyaline variety
with very little in the nature of calcareous deposits. In both genera this is probably
a primitive character.
THE SKULL OF CHLAMYDOSELACHUS
The vertebrate skull consists of the cranium and the visceral skeleton. The cranium
serves to protect the brain and certain sense organs: the olfactory organs, the eyes and
the membranous labyrinths. The visceral skeleton consists of a series of cartilaginous or
bony arches which partly surround the mouth and the pharynx. These arches comprise
the jaws or the mandibular arch, the hyoid arch, and the branchial arches or gill-arches.
The term cranium is sometimes used as a synonym for skull. The cranium is then divisi-
ble into two portions, the cerebral cranium or neurocranium, and the visceral cranium
or branchiocranium.
The Anatomy of Chlamydoselachus 351
THE CRANIUM
To illustrate various aspects of the cranium and some closely associated parts of the
endoskeleton of Chlamydoselachus, I have selected the excellent figures of Allis (1923)
for reproduction in my Plates I, and HI. In connection with his very detailed descrip-
tion of the skull, Allis has critically reviewed the work of his predecessors, Garman
(1885.2) and Goodey (1910.1). Of the work of Deinega (1909), Allis was probably un-
aware since he makes no reference to it.
Garman (1885.2, p. 8) writes thus of the “skull” (cranium) of his 1510-mm. specimen
of Chlamydoselachus:
The skull of the frilled shark is suggestive of immaturity; the thin walls, soft cartilage,
and large pores and foramina with thin edges around them, seem to be those of a young,
rather than an adult specimen. Compared with that of Heptabranchias [Heptanchus]
it agrees better with an embryo than an adult. Looking at it from above, its shape may be
likened to that of the body of a guitar, the vertebral column answering to the neck of the
instrument, and the narrow section between the orbits to the middle of its box... The
walls are very thin. In longitudinal section the thickness of floor and roof is comparatively
uniform. There isa marked contrast in this respect if compared with the skulls of Hex-
anchus and Heptabranchias, which in these portions are thick and irregular (see Gegenbaur,
1872, Das Kopfskelett der Selachier, Figs. 1 and 2, pl. IV)... The chamber is large, and the
brain small.
Allis (1923), whose excellent figures showing dorsal, ventral and lateral aspects of
the “‘neurocranium” of Chlamydoselachus are reproduced as my Plate I, says: “In dorsal
view [my Figure 1] it greatly resembles the neurocranium of Hexanchus (Gegenbaur,
1872), but its dorsal surface is even flatter.’ Also, in dorsal view the cranium of Chlamy-
doselachus is much like that of Heptanchus (Daniel, 1934, Figs. 45 and 46). According
to Allis the cranium of Chlamydoselachus differs from those of Hexanchus and Hep-
tanchus, and resembles those of Acanthias, Centrophorus and Scymnus (Gegenbaur,
1872, p. 39) in that the ventral surfaces (Figure 2, plate I) of the occipital and labyrin-
thine regions lie in the same level, and in that the eminence of the bulla acustica is found
on this ventral surface and not on the lateral surface (Figure 3, plate I) of the neurocranium.
This ventral position was considered by Gegenbaur to be secondary, due largely to
a greater development of the hyomandibular articular facet than is found in Hexanchus
and Heptanchus, or indeed in any other selachian skull figured by him.
All who have studied the matter agree that the notochord of Chlamydoselachus i is
continued as a slender strand of tissue in the base of the cranium as far forward as the
pituitary fossa. This is clearly shown in Garman’s (1885.2) Fig. B, nc, pl. VII; also in
my Text-figures 21 and 22 after Ayers, and in my Text-figure 30, p. 364, after Goodey.
It is faintly indicated in Deinega’s (1909 and 1924) Fig. 4, pl. II; in Goodey’s (1910.1)
Fig. 2, pl. XLII; and in my Figure 4, plate II (after Allis). This persistence of the anteri-
or portion of the notochord in the region of the basis cranii is a very primitive character.
To be sure, in all vertebrate embryos the notochord extends forward almost to the
352 Bashford Dean Memorial Volume
infundibulum, but in the higher vertebrates it disappears from the basis cranii during
later development.
In connection with his account of the persistence of the notochord of Chlamy-
doselachus in the region of the basis cranii, Goodey (1910.1, p. 543) makes the following
interesting statement: “The cartilage of the floor of the cranium in the region of its
junction with the vertebral column is thick and somewhat heavily calcified. It here
shows some indications of its probable vertebral nature, by the slight resemblance which
the calcification presents to the inverted V-formation found in the centra of the vertebral
column.” Ayers (1889) found more decided evidences (my Text-figures 21 and 22) of
Text-figure 21. Text-figure 22.
Sections through the skull of the frilled shark, Chlamydoselachus anguineus.
Text-figure 21. A transection of the basis cranii near the vertebral articulation, to show the fig
ure made by the calcareous sheath (and its processes) of the notochord, resembling a vertebra of
the trunk region.
cent., vertebral centrum (sheath of notochord); ch., chorda dorsalis; cran.cav., cranial cavity; ct., cartilage of the basis cranii;
n.p., neural process; tr_p., transverse process.
After Ayers, 1889, Fig. 8.
Textfigure 22. ft half of the hemisected cranium, to show the relations of the notochord and
cranial aorta to the basis cranii and to the pituitary prominence and space.
c., ctanial aorta; ch., chorda dorsalis (notochord); i.c., internal carotid artery; k., cephalic aorta; p.pl., pituitary plexus; pt.,
pituitary space; tr.c., transverse canal; III, third pair of aortic arches.
After Ayers, 1889, Fig. 3.
the persistence of the notochord (ch) and the rudimentary vertebral column in the basis
cranii of his specimen; but in view of the doubts that have been expressed concerning
the accuracy of many of Ayers’ observations on Chlamydoselachus, one should accept
this description and the accompanying figures with some reserve. In Hexanchus the
notochord (Text-figure 23, nc) persists in the posterior portion of the basis cranii, much
as in Chlamydoselachus.
My Figure 4, plate II, showing a medial view of the cranium of Chlamydoselachus,
should be compared with Text-figure 23, showing a similar view of the cranium of Hexan-
chus. The two figures are of interest chiefly because they show the foramina for the
exit of the cranial and occipital nerve roots.
The Anatomy of Chlamydoselachus 353
In Chlamydoselachus, any consideration of the cranium as a whole must take into
account its relation to the upper jaw (palatoquadrate) and to the suspensory apparatus,
on both of which it seems, to a considerable degree, to be molded. As one looks at the
skull from the side (Figure 5, plate II) he is impressed by the extraordinary length of the
jaws which begin posteriorly far behind the cranium and lie, when the mouth is closed,
in a nearly horizontal position. The ectethmoidal process projects over the outer surface
of the palatoquadrate, thus helping to hold it in place. The postorbital process of Chlamy-
doselachus is exceptionally large, but even when the mouth is closed it fails to reach the
tg.
Ole J ac.
i GP. V9.
t
m.
Cia. % ocn.
Text-figure 23.
Inner view of the right half of the skull of Hexanchus to show the cranial portion of
the notochord and the foramina for cranial nerves.
ac., foramen for auditory nerve; a.p., antorbital process; c., carotid foramen; ca., interorbital canal; gp.,
glossopharyngeal nerve; m., membrane over fontanelle; nc., notochord; o., optic nerve; ocn., spino-occipital
nerve; om., oculomotor nerve; 7., rostrum; tg., trigeminal nerve; tr., trochlear nerve; vg., vagus nerve;
vs., Occipitospinal nerve.
From Goodrich, 1909, Fig. 93, after Gegenbaur, 1872.
palatoquadrate. The nearly terminal position of the mouth is attained somewhat at
the expense of the cranium, for the rostrum is short and thin, though broad, and the
anterior third of the ventral surface of the cranium slants upward in such a way as
to allow the anterior part of the upper jaw to lie on a level with the posterior part of
the basis cranii. This is only one of several adjustments that make this creature, when
viewed from in front with its enormous jaws spread apart (Text-figure 2), seem to be
nearly all mouth. When this same specimen with the wide-open mouth is viewed from
the side, it appears that, in the process of opening the mouth, the upper jaw (and of
course, the cranium also) is elevated anteriorly, thus keeping the center of the mouth
cavity in line with the body. The site of this flexure is not in the occipito-vertebral
articulation, but in the vertebral column a few centimeters posterior to it. How this
flexion is accomplished I do not know, since the vertebral column has no articulations
354 Bashford Dean Memorial Volume
that seem to give any appreciable freedom of movement; but one should remember that
even a solid rod of cartilage is flexible.
In most selachians, when the mouth is closed the hyomandibular is directed down-
ward, outward or even forward; but in Chlamydoselachus it is directed posteriorly. As the
mouth opens, its angles spread apart so that the entire oropharyngeal cavity broadens;
this is made possible by the length and mobility of the hyomandibular. When the mouth
is closed, the hyomandibular is neatly folded between the palatoquadrate and the vertebral
column, its anterior end lying somewhat apart from the cranium and a little above the
level of the anterior end of the dorsal border of the hyomandibular facet (af in Figure 3,
plate I). This facet is a broad groove extending longitudinally for a considerable distance
on the posterior part of the lateral surface of the cranium. When the jaws are opened, the
anterior end of the hyomandibular must slide posteriorly along the facet, while the
posterior end swings laterad and somewhat ventrad through an angle of about 45°
(Garman, 1885.2). Thus the articulation of the hyomandibular with the cranium is
a sliding joint of unusually loose construction, aiding greatly in the range of movement
of the hyomandibular. This peculiar hyostylism of the skull, together with the nearly
terminal position of the mouth, the long jaws and indeed the entire complex of adjust-
ments that gives Chlamydoselachus its enormous gape, are to be viewed as comparatively
recent adaptations of a highly specialized character. Goodey (1910.1, p. 550) says of the
jaws of Chlamydoselachus that “their disposition relative to the cranium is quite different
from that found in any Selachian whose skull I have been able to examine or see a figure
of. It resembles nothing among the Vertebrates so much, perhaps, as the general dispo-
sition of the jaws in certain of the Ophidia.”
Allis has described a palatal process of the palatoquadrate which serves as a support
for the soft parts of the horizontal palatine shelf. “The palatine process of Chlamy-
doselachus .. . isa curved flat plate of cartilage, of nearly even width, that projects antero-
mesially beneath the anterior end of the neurocranium” (Allis, 1914, p. 354). The
horizontal palatine shelf, which is evidently a homologue of the maxillary breathing valve
of certain teleosts, is fully described by Gudger and Smith (1933, p. 269).
The cartilaginous lateral wall of the suprapalatine recess is perforated, on either
side, by the nasal fontanelle (naf, Figure 2, plate 1). In its position and relations the
nasal fontanelle is, apparently, the strict topographical homologue of the fenestra choanalis
of Amphibia (Allis, 1913 and 1914). In its natural state the nasal fontanelle of Chlamy-
doselachus is closed by a tough membrane (Allis, 1923, p. 132) which appears to be a part
of the cranium. This membrane is distinct from the mucous membranes lining the nasal
capsule and the mouth. The membrane evidently represents unchondrified portions of
the subnasal plate and the nasal capsule. ‘“The nasal cavity of Chlamydoselachus is
thus separated from the suprapalatine recess by membranous and mucous tissues only,
and if these tissues were to be secondarily [sic] perforated . . . an internal nasal aper-
ture would be formed which would lie directly above the horizontal palatine shelf”
(Allis, 1914, p. 355).
The Anatomy of Chlamydoselachus 355
The postorbital process closely approaches the palatoquadrate but does not articulate
with it. The orbital process of the palatoquadrate is unusually large and projects far
into the deeper portion of the orbit, where it articulates with a large facet on the ventral
edge of the anterior wall of the orbit. The orbital process forces the eyeball away from
the medial wall of the orbit. These relations must change considerably when the pharynx
is expanded, on account of the spreading of the jaws posteriorly and the shifting of the
angles of the jaws ventrad (note the space between palatoquadrate and cranium in Text-
figure 84, p. 429). The only articulation of the palatoquadrate with the cranium is by
way of the orbital process, which is very loosely attached to the cranium.
The eyestalk of Chlamydoselachus is a slender rod of cartilage which projects from
the anterior edge of the trigemino-pituitary fossa and curves around the posterior surface
of the capsular sheath of the orbital process of the palatoquadrate (Figure 2, plate I;
Figures 5 and 6, plate I). Its distal end hasa sliding articulation with the medial surface of
the eyeball, without being attached to it. According to Gegenbaur (1872) the eyestalk
of the plagiostomes does not belong genetically to the eye, neither does it, except in its
basal portion, belong to the chondrocranium. In all the plagiostomes, the basal portion
of the eyestalk is of firmer tissue than the remainder of the stalk, which is always of softer
tissue than the chondrocranium. Gegenbaur suggested that the eyestalk (excepting
its basal portion) might be a part of the visceral skeleton that had secondarily acquired
relations with the eyeball. Allis (1923) cites Dohrn’s suggestion that it might represent
a part of a premandibular visceral arch, and recalls his own earlier suggestion (Allis,
1914, p. 365) that “the eyestalk is a modified branchial ray or rays, of a mandibular or
premandibular arch, that has secondarily acquired relations to the eyeball.” While such
explanations are highly speculative, an origin from a branchial ray of the mandibular
arch seems the most plausible. That the eyestalk originated from some pre-existing
cartilaginous structure seems indicated by this statement from Allis (1914, p. 347):
The eyestalk is certainly a retrograding and archaic structure, as its varying importance
and wide distribution clearly indicate, and it seems certain that it could not have been de-
veloped independently, merely as a support to the eyeball, a function it so inefficiently
fulfils except in certain rays (Harman). And that it was developed as a point of attachment
for the recti muscles seems improbable because it actually fulfils that function, so far as I can
find, only in Chlamydoselachus (Hawkes, 1906) and possibly in Zygaena.
At the bottom of the endolymphatic fossa (ef, Figure 1, plate I) are four apertures,
two on each side, described by Goodey (1910.1) and by Allis (1923, p. 155). Each anterior
aperture is a foramen ductus endolymphaticus, or aqueductus vestibuli, and affords
passage for the ductus endolymphaticus. Each posterior aperture leads directly into the
perilymphatic cavity of an ear, and is the so-called fenestra ovalis of Scarpa, or the fenestra
vestibuli cartilaginei of Weber. In the natural state this aperture is closed by a membrane.
In Chlamydoselachus and in Mustelus, the fenestra vestibuli lies immediately above the
apex of the posterior membranous semicircular canal of the ear.
356 Bashford Dean Memorial Volume
A rear view of the skull (Figure 6, plate II) shows the foramen magnum (fm), and
beneath it a small perforation, not labeled, for the extension of the notochord forward
into the basis cranii. The figure shows also a posterior view of the hyomandibular
articular facet (af), the postorbital process (pop), the ectethmoidal process (ecp), and the
eyestalk (es).
As in other elasmobranchs, the brain does not fill the cranial cavity, which is shown
from the dorsal aspect in Figure 7, plate III. This figure shows also the olfactory capsules,
partly dissected, lying on each side of the broad rostrum.
THE VISCERAL SKELETON
In most elasmobranchs there are seven visceral arches: the mandibular, the hyoid,
and five branchial arches. In Chlamydoselachus and the notidanids there are additional
branchial arches making a total of eight visceral arches in Chlamydoselachus and Hexan-
chus, and nine in Heptanchus.
Since the mandibular arch and the hyoid arch are usually regarded as derivatives
of primitive branchial arches, some embryologists use the term branchial arch for each
member of the entire series of visceral arches, and number them consecutively. In com-
parative anatomy it is more common to designate the mandibular arch and the hyoid arch
as such, and restrict the name branchial arch to the succeeding arches, which are numbered
separately. Thus, the third visceral arch is the first branchial arch.
In Chlamydoselachus, as in other elasmobranchs, the mandibular arch (Figure 5,
plate II) is divided into an upper palatoquadrate or pterygoquadrate segment, and a lower
mandibular segment (Meckel’s cartilage). The articulation between these two elements
is of a simple type, figured by Allis (1923) in his Pl. XII. The ligaments connecting the
palatoquadrate with the mandible, and the mandibular arch with the hyoid arch, are
shown by Allis (1923) in his Pls. X and XI. Allis (1923, p. 149) states that the orbital
process of the palatoquadrate has a capsular sheath, and (pp. 208 and 209) refers to
a “somewhat ligamentous portion of the connective tissue that attaches the capsular
sheath to the anterior wall of the orbit.” Garman (1885.2, p. 10) writes: “Some of the
most prominent differences between Chlamydoselachus and the notidanids are to be seen
in the attachments and articulations of this cartilage [the palatoquadrate].”
As compared with the same structures in other sharks, the jaws of Chlamydo-
selachus (Text-figure 24; Figure 5, plate II) are slender. This slenderness stands in marked
contrast with the condition found in Heptanchus (Daniel, 1934, Fig. 48), and is correlated
with a decided difference in the character of the teeth. In Chlamydoselachus, much
more than in Heptanchus, the jaws resemble branchial arches.
The anterior labial cartilage (Figure 5, plate IJ) gives insertion to a long and stout
ligament attached to the cranium. From this ligament a series of ligamentous strings
are sent off to the upper lip. The posterior upper labial has no direct supporting relations
to the upper lip, but the posterior lower labial or mandibular labial gives attachment, at
its posterior end, to the tendon of the protractor anguli oris, and from its point of artic-
The Anatomy of Chlamydoselachus 357),
ulation with the posterior upper labial it extends forward, along the ventral edge of
the mouth, strongly attached to the inner surface of the dermis of the lower lip (Allis,
1923). The presence of a mechanism for strengthening and mobilizing the soft tissues
at the angles of the mouth supports my contention that Chlamydoselachus seizes and
swallows large prey.
Text-figure 24.
Ventral view of the visceral skeleton (three-fourths natural size) of Garman’s first specimen
of Chlamydoselachus. The branchial rays are omitted from all arches except the hyoid.
b-br, basibranchial; b-hy, basihyoid; br-r, branchial ray; c-br, ceratobranchial; c-hy, ceratohyoid; e-br, epibranchial; h-br,
hypobranchial; mk, mandible or Meckel’s cartilage; p-br, pharyngobranchials.
After Garman, 1885.2, Pl. IX.
The homologies of the labial cartilages of elasmobranchs are obscure. Pollard (1895)
considered the labial cartilages to be the remains of the skeletal supports of a set of
primitive oral cirrhi such as are found still in Amphioxus and in myxinoids. Others,
like Sewertzoff (1916), believe the labial cartilages to represent vestiges of the visceral
arches of two segments in front of the mandibular. Concerning this view Goodrich
(1930, p. 448) writes as follows: “Against the theory maintained by Sewertzoff it may
be urged that there is no good evidence of the existence at any time of gill-pouches,
arches, etc., anterior to the mandibular, that the labials are too superficial to be of visceral
nature, and that the supposed vestiges of gill-pouches corresponding to them apparently
occur anteriorly to the pharynx (endodermal gut). Possibly the labials are merely
secondary in Gnathostomes and of no great morphological importance.” The labials
may be tentatively classified as extravisceral cartilages of the mandibular arch, in series
with the extrahyoids and the extrabranchials.
358 Bashford Dean Memorial Volume
Neither Garman (1885.2) nor Goodey (1910.1) found any spiracular cartilages in the
specimens dissected by them, and Furbringer (1903, p. 389) found only a single spiracular
cartilage in his specimen. Allis (1923, Fig. 22, pl. XI) found three small nodules of
cartilage situated in a loose prespiracular band of connective tissue (which does not have
the same relations as a spiracular ligament) on each side of one specimen. The cartilages
are described by Allis (1923, p. 169) as follows:
These cartilages present strikingly the appearance of being rudiments of the basal
portions of three adjoining branchial reys related to the mandibular arch, and, like the single
spiracular cartilage described by Furbringer in the one specimen examined by him, they lie
lateral, and hence morphologically anterior, to the artery of the arch. They lie posteroventral
to that part of the spiracular canal that bears the pseudobranchial filaments and in no sup
porting relations whatever to them, and hence, while possibly representing persisting
rudiments of mandibular reys, they may not be true spiracular cartilages, for Gegenbaur
(1872, p. 198) says that in all the Plasiostomi in which it is found, the spiracular cartilage
always lies in the anterior wall of the spiracular canal, and that, where there is a pseudobranch,
the filaments of that organ lie directly upon the cartilage.
Evidently Daniel (1934, p. 63) considers that the dorsal segment of the second visceral
arch of Chlamydoselachus is not a true hyomandibular, since he writes of it that “the
dorsal segment is on its way to become a hyomandibula or suspensorium.” According to
Allis (1923) there is no ligament connecting the hyomandibular with the palatoquadrate;
there are, however, ligaments connecting the hyomandibular with the mandible (Meckel’s
cartilage) in the region of the quadrato-mandibular articulation, and a broad capsular
ligament binding the hyomandibular strongly to the cranium. The sliding articulation
of the hyomandibular with the cranium has already been described. The homologies of
the hyomandibular of fishes are discussed by Allis (1915) and by Gregory (1933, pp.
80-82). Woodward (1921, p. 39) regards the hyostylic suspension of the jaws, found in
nearly all modern sharks and skates, as a condition secondarily attained, while the primi-
tive mode of suspension of the jaws is amphistylic, as in Cladoselache (and in the noti-
danids). One may well be puzzled to decide whether the peculiar mode of suspension of
the jaws of Chlamydoselachus is amphistylic or hyostylic. It does not conform fully to
either type, but comes nearer to being hyostylic. Goodey (1910.1, p. 544) states un-
reservedly that “the suspension of the jaws is hyostylic.~
The hyomandibular of Chlamydoselachus bears nine (Garman, 1885.2) or more
cartilaginous branchial rays. Goodey (1910.1) shows, in his Fig. 1, pl. XLII, ten branchial
rays attached to the hyomandibular and one branchial ray slightly detached from it.
Allis (1923), in his figure reproduced as my Figure 5, plate II, shows nine branchial rays
attached to the hyomandibular and five or six others more or less detached but evidently
related to it.
The ceratohyoids (Text-figure 24, chy) parallel the mandibular or Meckelian carti-
lages (mk) and are intermediate in size between these and the ceratobranchials (cbr).
Viewed from below, as in Garman’s figure, the visceral skeleton of Chlamydoselachus
The Anatomy of Chlamydoselachus 359
presents a striking picture of gradation between jaws and gillarches. A more nearly
perfect gradation is exhibited in Dean’s reconstruction of Cladoselache fyleri, shown
in my Text‘figure 25. Since the ceratohyoids, as well as the hyomandibulars, of
Chlamydoselachus bear branchial rays (my Figure 5, plate II), the hyoid arch can scarcely
be derived from the velum of an amphioxid ancestor as alleged by Ayers (1931). In
Heptanchus (Daniel, 1934) the hyoid segment possesses an extravisceral cartilage, not
present in Chlamydoselachus.
All the branchial arches of Chlamydoselachus, except-
ing the sixth and the vestigial seventh, bear branchial rays
(Text-figure 77; and Figure 8, plate III). These are very
slender rods of cartilage, attached at one end to a branchial
arch, and supporting the gillseptum. Goodey (1910.1)
states that in his two specimens, male and female respective-
ly, the greatest number of rays occurs on the hyoid arch,
and as one proceeds posteriorly the number gradually de-
creases. His tables showing the number of rays on the
right and left sides of each arch, from the hyoid to the fifth
branchial arch inclusive, support his statement. The same
trend is shown in Collett’s (1897) table showing the num-
ber of rays for each branchial arch (one side only?), from
the first to the sixth inclusive, in his large specimen; but
it is probable that Collett’s first arch, bearing nineteen
rays, is really the hyoid arch, and his sixth branchial arch,
bearing eight rays, is really the fifth.
In each of the first five branchial arches of Chlamy- Text-figure 25.
doselachus there is a dorsal extrabranchial cartilage, de- Reconstruction of the underside
scribed by Furbringer (1903) and by Allis (1923, Fig. 49. ofthe skull of 2 Devontanishavk;
S ; fara Cladoselache fyleri, showing low-
pl. XVIII). In Furbringer’s Figs. 31, 32, 33, Taf. XVIII, the Sr rawmuintecrion ait neilbancten
extrabranchial cartilages appear like detached or fragmented NgeoDexn, 1099) Fig. 6
branchial rays, usually small.
The basibranchials and hypobranchials constitute the most variable part of the
visceral skeleton of Chlamydoselachus. Viewed as departures from an easily recognized
type, these variations are interesting. In none of the specimens of Chlamydoselachus
that have been described is there a distinct basibranchial associated with the first pair
of ceratobranchials. To be sure, Garman (1885.2, p. 11) enumerates a first basibranchial
in his series, but this would be a second if the series were complete. In order to make
comparisons, one must revise his enumeration to correspond with that used by Goodey
(1910.1) and others. With this change of labels, Garman describes and figures separate
second and third basibranchials (my Text-figure 24). The fourth basibranchial is fused
with the corresponding hypobranchials, is obliquely and indistinctly divided, and is closely
joined with the fifth which is fused with the sixth and indistinguishable from it save by
360 Bashford Dean Memorial Volume
its position and relations. The hypobranchials of the first pair are small and are situated
dorsal to the medial ends of the ceratohyoids. The second and third pairs of hypo-
branchials are distinct and well developed. The fifth and sixth pairs of hypobranchials
are mere rudiments fused with the basibranchials.
Furbringer’s specimen (1903, Fig. 18, Taf. XVII) presents several features that are
different. A small median posteriorly directed prominence fused with the basihyoid
may represent the first basibranchial, and a pair of posterolateral processes of the basihyoid
probably represents the first pair of hypobranchials. The second basibranchial appears
to be entirely absent, but there is a pair of second hypobranchials. The third basibranch-
ial is distinct from the fourth basibranchial, but is fused with the fourth pair of hypo-
branchials. The fourth basibranchial is distinct from the fifth, but the fifth and sixth
basibranchials are fused together. The fifth and sixth pairs of hypobranchials are not
identified with certainty. There is a vestigial seventh branchial element. Some features
of Furbringer’s drawing are obscure, so that it is not suitable for reproduction here.
Goodey (1910.1) described and figured (my Text-figure 26a) a small posteriorly
projecting prominence (bbr. 1?) on the basihyoid which, as in Furbringer’s specimen,
probably represents a fused first basibranchial. Otherwise, Goodey’s drawing more
closely resembles that of Garman (1885.2). There are, however, some differences. “The
two lateral prominences [of the basihyoid], also at the posterior end, no doubt represent
the hypobranchials of the first branchial arch” (Goodey, 1910.1, p. 545). In Garman’s
figure (my Text-figure 24) the hypobranchials of the first branchial arch appear to be
separate elements over-lapped by the ceratohyoids.
Garman (1913) described and figured (my Text-figure 26s) this region of the visceral
skeleton in still another specimen. Here, there is no posterior projection of the middle
part of the basihyoid to represent a vestigial first basibranchial, but the other basibran-
chials are more numerous and regular than in any other specimen that has been figured.
There are five elements represented in this series, of which the fourth probably represents
the combined fifth and sixth basibranchials, while the slender posterior element may
belong to the vestigial seventh branchial arch discovered by Furbringer (1903). The
first pair of hypobranchials (hbr. 1) is represented by posterolateral processes of the basi-
hyoid, while one member of both the second and the fourth pairs of hypobranchials
is fused with the corresponding basibranchial. The hypobranchials of the sixth pair
are small and are displaced somewhat posteriorly. The most posterior pair of cartilages
(v. br. a. 7) presumably represent ceratohyoids of the seventh arch.
Allis (1923) agrees closely with Garman (1885.2) in his description and portrayal
of the basibranchials, but in the fourth branchial arch of his specimen he finds one of the
hypobranchials distinct and independent while the other is fused with the fourth basi-
branchial to form a single median cartilage with a lateral process on one side only. This
fused hypobranchial is well shown in dorsal view (Figure 8, plate III), but is only partly
shown in a ventral view (Figure 9, plate III). The former figure shows also a pair of
rudimentary nodules representing the sixth hypobranchials, and both figures show a pair
of rudimentary seventh hypobranchials.
The Anatomy of Chlamydoselachus 361
Deinega’s otherwise excellent figure (1909 and 1923, Fig. 5, pl. II) of the visceral
skeleton of Chlamydoselachus does not show clearly the limits and the relations of all
the basibranchials and hypobranchials, hence it cannot be used for comparison.
[Se nee
\-hbr.1(?)
bbr2X% - ----
cbr 2. -
Vo ae
BINS
4K -hbré
bree + FERRE
Text-figure 26.
Ventral views of the median portions of the branchial skeletons of two specimens of
Chlamydoselachus to show variations.
A—Dissection by Goodey (1910.1) of a specimen in the University of Birmingham.
bbr.1(?)-6, basibranchials of the first (?) to the sixth arch; bh., basihyoid; cbr.1-6, ceratobranchials of the first to
the sixth arch; f., foramen; hbr. (1) (?)-6, hypobranchials of the first to the sixth arches; th.c., thyroid con-
cavity; vba7(?), vestigial seventh branchial arch.
Redrawn, with some changes in labels, after Goodey, 1910.1, Fig. 6, pl. XLIII.
B—Dissection by Garman (1913) of his second specimen in the Museum of Comparative
Zoology. The original is without lettering.
bbr.2, 5 and 6 (?), basibranchials; bh., basihyoid; cbr.4 and 6, ceratobranchials; chy., ceratohyoid; f., foramen in
basihyoid cartilage; hbr.1,2 and 6, hypobranchials; v.br.a.7, vestigial seventh branchial arch.
After Garman, 1913, Fig. 6, pl. 59.
362 Bashford Dean Memorial Volume
Text-figure 27. Text-figure 28.
Dorsal and ventral views of the visceral skeleton of the notidanid shark, Heptanchus.
Text-figure 27. Branchial skeleton of Heptanchus sp., in dorsal view.
EVIL, first to seventh branchial arches; C, copula or basihyaid; CI, fused sixth and seventh basibranchials; c I—c V, second
_ to fifth bastbranchals; ky, ceratohyoid; 1, hypobranchials; 2, ceratobram ; 3, epibranchials;
After Gegenbaur, 1872, Fis. 1, Taf. XVI
Text-figure 28. Visceral skeleton of Heptanchus maculatus, ventral aspect.
4, pharyngobranchials.
bb.2, second basibranchial; bh., basihyoid; cb., ceratobranchiels; ch., ceratohyoid; hb., hypobranchials; mp., median piece.
After Daniel, 1934, Fig. 50.
The vestigial seventh branchial arch in Chlamydoselachus was first described and
figured by Furbringer (1903, p. 409 and Fig. 18, pl. XVII). In his specimen it consisted
of a single small rod of cartilage on each side. In a young specimen described by Hawkes
(1907) it consisted of four small pieces on one side and two on the other. In another
specimen, an adult, examined by Hawkes there were only two pieces “in a similar posi-
tion,” the larger one equal in length to the combined four pieces found in the smaller
specimen. Ina third specimen studied by Hawkes a seventh branchial arch was entirely
lacking. Of two specimens examined by Goodey (1910.1), in one this arch was lacking,
in the other it was represented (Text-figure 26a, vba. 7?) by “a pair of small, segmental
tapering pieces lying on the ventral side of the last basibranchial at the bases of the
sixth ceratobranchials.” In a specimen described and figured by Garman (1913) the
vestigial seventh arch (my Text-figure 26s) is represented by a pair of cartilages consider-
ably larger than any described or figured in other specimens. The seventh branchial
arch of a specimen studied by Allis is shown in my Figures 8 and 9, plate III, and is
described by Allis (1923, p. 179) as follows:
From the left posterolateral comer of the sixth basibranchial, a chain of small thin nodules
of cartilage extends posteriorly and represents the vestigial seventh ceratobranchial... On
the right side of the head this chain of nodules is represented by a process of the basibranchial.
Wedged in between the base of this process and the distal end of the sixth ceratobranchial
The Anatomy of Chlamydoselachus 363
there is a small nodule of cartilage, a similar nodule being ‘found on the opposite side of the
head wedged in between the basal one of the chain of three small nodules and the related
ceratobranchial. These two little nodules are, in position and appearance, strict serial
homologues of the two nodules that represent the proximal ends of the sixth hypobranchials,
and they are accordingly quite probably the corresponding ends of the seventh hypobranchials,
the posterior process of the large cardiobranchial then being the seventh basibranchial.
A comparison of all the available figures of the seventh branchial arch in Chlamy-
doselachus shows that this arch is extremely variable and is never fully developed. Iam
inclined to think that phylogenetically it is in process of disappearance rather than in
process of development. A rudimentary ninth branchial arch is present in Heptanchus
(Daniel, 1934, Fig. 50s).
It is in the ventral portion of the branchial skeleton of selachians that the greatest
amount of variation takes place. A complete series of basibranchials and hypobranchials,
without fusion, is presumably the primitive condition, but so far as I know this condition
is not fully realized in any living fish. Chlamydoselachus and the notidanids probably
come the nearest. Gegenbaur’s drawing (1872, Fig. 1, pl. XVIII) of the branchial skeleton
of Heptanchus is here reproduced as Text-figure 27. The first basibranchial is lacking
and the sixth and seventh are fused together. If one compares Furbringer’s drawing of
Heptanchus (1903, Fig. 29, Taf. XVIII), and Daniel’s illustration (1934, Fig. 50a) re-
produced as my Text-figure 28, one finds in the basibranchials of Heptanchus quite as
much irregularity as I have noted for the same structures in Chlamydoselachus. On the
other hand, in Heptanchus the hypobranchials form a more nearly perfect series, especially
if one considers the vestigial first and seventh pairs figured by Daniel (my Text-figure 28).
In Hexanchus (Gegenbaur, 1872, Fig. 2, Taf. XVIII; Furbringer, 1903, Fig. 19, Taf.
XVII), the basibranchials resemble those of Chlamydoselachus as figured by Goodey
(my Text-figure 26a). In respect to both basibranchials and hypobranchials, Chlamy-
doselachus and the notidanids are primitive, yet so variable that they seem to possess the
materials for a rapid evolutionary change.
Text-figure 29.
Longitudinal section of vertebral column and notochord in the cervical
region of Chlamydoselachus.
ch, notochord; in, interdorsal; is, interspinous process; nc, neural canal.
After Garman, 1885.2, Fig. 3, pl. X.
364 Bashford Dean Memorial Volume
NOTOCHORD AND VERTEBRAL COLUMN
In Chlamydoselachus, the notochord is persistent to a degree not found in the higher
elasmobranchs. Perhaps in no other living shark does the notochord of the adult retain
its primitive condition through so large a portion of its length. The notochord of Chlamy-
doselachus extends from the pituitary fossa of the basis cranii to the extreme tip of the
tail. In the basis cranti it is very slender, but elsewhere it is a fairly stout rod.
Text-figure 30.
Vertical longitudinal section of the anterior end of the vertebral column in a large female
Chlamydoselachus, showing calcified cyclospondylous centra.
bd., basidorsal; cal., calcification; c.c.5, cyclospondylous centrum of the fifth cervical vertebra; ch., notochord;
ch.s., chordal sheath; d.f., dorsal root foramen; i.d., interdorsal cartilaginous element; s.bd., suprabasidorsal;
s.d.l., supradorsal ligament; so.4, spino-occipital foramen; v.f., ventral root foramen; X, foramen for tenth
cranial nerve.
After Goodey, 1910.1, Fig. 10, pl. XLII.
In the cervical (cephalic, according to Goodey’s nomenclature) and main caudal
regions the notochord of Chlamydoselachus shows pronounced metameric constrictions
(Text-figures 29, 30 and 31) due to inward projecting thickenings of its sheath. In the
trunk region and in the region of the dorsal and anal fins, the constrictions of the noto-
chord are very slight (Text-figures 32 and 33); according to Garman (1885.2, Fig. 2, pl. X)
they are limited to the ventral portion of the notochordal sheath and do not extend to
the notochord proper. The metameric constrictions of the notochord are of interest
because they occur in connection with the formation of rudimentary cyclospondylous
centra. In Chlamydoselachus we find initial stages in the formation of these centra.
Similar constrictions of the notochord occur in Heptanchus. For the cervical region
and near the base of the anal fin, these are illustrated by Text-figures 34 and 35. In the
trunk region of Heptanchus the constrictions of the notochord are slight (Daniel, 1934, p.
48). In Hexanchus (Regan, 1906.2, p. 740) the notochord is constricted by annular
thickenings of the cartilaginous sheath, without calcification such as occurs in Hepta-
branchias (Heptanchus) where the notochord is constricted vertebrally by a series of
calcified rings.
On page 351 I have described the continuity of the vertebral portion of the notochord
with its more slender portion imbedded in the cranium. All observers agree in empha-
sizing the firmness of the attachment of the vertebral column to the cranium. Goodey
The Anatomy of Chlamydoselachus
Text-figure 31.
Surface and sectional views of a portion of the vertebral column (x 1.25) from the main-
caudal region of Chlamydoselachus.
A—Surface view showing ridged extensions of the arcualia around the notochord.
bu., basiventral; c.c., cyclospondylous centra; ch.s., chordal sheath; h.s., haemal spine; i.bd., imperforate basi-
dorsal; i.id., imperforate interdorsal; iv., interventral; p.bd., perforate basidorsal; p.id., perforate interdorsal.
After Goodey, 1910.1, Fig. 15, pl. XLIV.
B—Vertical longitudinal section (with anterior and posterior ends reversed) showing
calcified cyclospondylous centra of two sizes.
bv., basiventral; h.c., haemal canal; h.s., haemal spine; l.c.c., larger cyclospondylous centrum; ne.c., neural canal;
s.c.c., smaller cyclospondylous centrum.
After Goodey, 1910.1, Fig. 16, pl. XLIV.
td,30 s..l. us. def.
Text-figure 32.
A portion of the vertebral column (x 1.5) from the trunk region of Chlamydoselachus.
Note the rudimentary ribs.
a.ch.s., annulation in the chordal sheath; bd., basidorsal; bv., basiventral; d.f., dorsal foramen; id.,
interdorsal; iv., interventral; rb., rib; s.d.]., supradorsal ligament.
After Goodey, 1910.1, Fig. 11, pl. XLIV.
365
366 Bashford Dean Memorial Volume
(1910.1, p. 554) states: “The vertebral column is fused to the cranium quite firmly, so
that but slight articulation is possible between the two.” On this point Allis (1923,
p. 161) writes:
In my specimens of Chlamydoselachus there is no continuity of the cartilage here, so far as
I can determine from macroscopic examination. The opposing surfaces of the chondro
cranium and first vertebra are closely applied to each other, and there is but little movement
possible between them, but a certain amount of lateral movement is nevertheless possible, and
the two articular surfaces can always be separated without breakage of the cartilage.
s.d.L. bd.cs way osibd an UH ag.
PAI
Text-figure 33.
A portion of the vertebral column (x 1.4) of Chlamydoselachus, in the
region of the dorsal and anal fins, showing the transition from mono-
spondylous to diplospondylous vertebrae.
a.ch.s., annulation in the chordal sheath; bd.69, basidorsal no. 69; bv., basiventrals; d.f.,
dorsal foramen; iv., interventral; n.70 and n.72, neuromeres 70 and 72 respectively; s.bd..
supra-basidorsal; s.d.]., supradorsal ligament; v-f., ventral foramen.
After Goodey, 1910.1, Fig. 12, pl. XLIV.
The vertebral column of Chlamydoselachus is of a very simple elasmobranch type.
The best description is that of Goodey (1910.1), and I shall base my treatment mainly on
his account. There is a long central cylinder, which comprises the notochord together
with its enlarged sheath. Above the chordal sheath there is a series of cartilaginous
vertebral elements arching over the spinal cord. These elements, comprising the neural
arches or the dorsalia, are classified by Goodey, using Gadow’s (1895) nomenclature, as
follows: basidorsals, interdorsals and supra-basidorsals, the last-named being segmented
off from the apices of the basidorsals. Below the chordal sheath there is another series
of vertebral elements, the ventralia, consisting of basiventrals, interventrals, ribs, and
haemal spines in the caudal region. These various elements making up the vertebral
column are illustrated in Text-figures 30-33 inclusive. There is an elastic supradorsal
ligament which extends from the cranium to a point just posterior to the dorsal fin.
This must greatly strengthen the column.
There is no detailed account of the histological structure of the chordal sheath in
Chlamydoselachus, but in Heptanchus (Daniel, 1934, p. 48, and Fig. 52 reproduced as my
The Anatomy of Chlamydoselachus 367
Text-figure 34) it is composed of three concentric layers as follows: ‘The outermost of
these layers is relatively thin and consists of cartilage; within this cartilage is a second
and lighter broad area which appears to be made up of transverse fibers. Within this
second layer and bounding the notochord is a third layer of a white tissue. At regular
intervals the third layer forms septa which produce the regular constrictions in the
central part of the notochord. It will be observed that the septa are more pronounced
ventrally than dorsally, and that they pass intra-centrally.” The development of the
sheath is discussed by Daniel (1934, p. 70).
In a large female specimen of Chlamydoselachus described by Goodey (1910.1) the
first eleven vertebrae possess ring-like thickenings of the chordal sheath, which project
inward in such a manner as to constrict the notochord and make it appear somewhat
Text-figure 34.
Sagittal section through sixth to eighth
segments of the vertebral column of
Heptanchus maculatus, showing struc-
ture of the chordal - sheath.
chd, notochord; iz, inner zone, mz, middle zone,
and oz, outer zone, of the notochordal sheath;
nc, neural canal; s, septum constricting notochord.
After Daniel, 1934, Fig. 52.
like a string of beads (Text-figure 30). The soft notochordal tissue gradually becomes
obliterated from the intervertebral spaces as it approaches the skull, so that in the space
between the first centrum and the cranium soft tissue is not present at all (Goodey,
1910.1, p. 555). This is apparently not true of Garman’s large specimen (Text-figure 29)
in which the notochord (ch) is nowhere completely interrupted by the constrictions of
the chordal sheath. Continuing my account of the cervical region in Goodey’s large
specimen: Each constriction appears below a basidorsal, so that the constrictions are
intravertebral. Each thickening of the chordal sheath possesses a calcification, as shown
by the deeply shaded areas in Text-figure 30, c. c., and in a median vertical longitudinal
section of a single vertebra these calcified areas appear like two Vs placed point-to-point.
Thus each centrum has the form of a short cylinder constricted round its middle. There
are no articular surfaces, nor even septa, separating any two successive centra; the
notochordal sheath is continuous and the intervertebral spaces are filled in by successive
bead-like segments of the notochord. The relations of the notochordal sheath are
shown somewhat better in a smaller and presumably younger specimen studied by
Goodey (1910.1, Fig. 9, pl. XLIII), in which some of the constrictions are not so well
developed and the calcifications are not complete.
In the unusually long trunk region of Chlamydoselachus, the notochord (Text-figure
32) is almost uniform in diameter; nevertheless, according to Goodey, it shows slight but
unmistakable signs of segmentation. This segmentation is described by Goodey as follows:
368 Bashford Dean Memorial Volume
The segmentation is shown by a difference in the appearance of the chordal sheath
along lines corresponding in position to the ends of the basidorsals. At these points there
appear to be narrow rings or annulations of the notochord as shown in Fig. 11 [my Text-figure
32]. In a view of the cut surface of a vertical longitudinal section of a portion from this
region, no apparent constrictions of the notochord are found to correspond with the external
segmentation of the chordal sheath. The interior of the chord presents a fairly uniform
appearance, as was noted by Garman. If, however, a horizontal longitudinal section be made
of the notochord, a regular sequence of constrictions of the chordal sheath is at once apparent.
Each of these occurs beneath a basidorsal, and extends between two consecutive segmen-
tation marks on the exterior of the chordal sheath. Each takes the form of a bulging inward
of the sheath, so that a slightly pinched-in cylinder is formed.
There are no calcifications of the notochordal sheath in the trunk region of Chlamy-
doselachus. Rudimentary ribs are shown in Text-figure 32.
The cervical and trunk regions are typically monospondylous, i. e., each “neuromere”’
(Goodey’s terminology) is made up of one of each kind of vertebral element: basidorsal,
interdorsal, supra-basidorsal, basiventral and interventral. The foramina for the spinal
nerves do not occur between the dorsalia but are actual perforations of the basidorsals
and interdorsals. In the monospondylous regions each basidorsal transmits a foramen
for a ventral root, and each interdorsal, one for a dorsal root. At the seventieth neuro-
mere, Goodey found an interesting transition from the monospondylous to the diplo-
spondylous condition (my Text-figure 33). There is a doubling of the number of basidor-
sals, interdorsals and supra-basidorsals, but only the posterior interdorsals and basidorsals
of each neuromere contain foramina for the exit of the roots of spinal nerves. In the
seventy-second neuromere the monospondylous condition recurs dorsally, but the
ventral elements are diplospondylous. The diplospondylous condition characteristic
of the caudal portion of the vertebral column in sharks probably arises out of the mono-
spondylous by a process of fragmentation of the primitive cartilaginous vertebral
elements.
Goodey does not tell us precisely where, with reference to external features, the
transition from the monospondylous to the diplospondylous condition in Chlamydosela-
Text-figure 35.
Lateral view of the spinal column of Heptanchus maculatus in the region of transition from the
monospondylous to the diplospondylous condition, near the base of the anal fin.
chd., notochord; f.d., foramen for dorsal nerve root; f.v., foramen for ventral nerve root; h.a., haemal arch; r., rib;
s., septum constricting notochord; 44-60, vertebrae.
After Daniel, 1934, Fig. 53.
The Anatomy of Chlamydoselachus 369
W108 109 nito
TM LADLE DTS: we
ee
Wii
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Text-figure 36.
Terminal caudal portion of the vertebral column of Chlamydoselachus,
showing heterospondyly.
ch, notochord; hs, haemal spine; n 108—n 112, neuromeres.
After Goodey, 1910.1, Fig. 17, pl. XLV
chus occurs; but from a comparison of Text-figure 33, after Goodey, with Text-figure 48,
p. 378, after Garman, it appears to be in the region of the dorsal and anal fins. Here, the
condition of the notochord and of the chordal sheath (Text-figure 33) is similar to that
in the trunk region (Text-figure 32). In Heptanchus (Daniel, 1934, p. 48) the transition
occurs at about the fifty-sixth segment dorsally, and somewhat farther forward ventrally
(my Text-figure 35); this region lies dorsal to the base of the anal fin.
In the main caudal region of a large female specimen of Chlamydoselachus described
by Goodey (1910.1), the diplospondylous condition is well established (my Text-figure
31). The constrictions of the chordal sheath are of two sizes, the larger more calcified
ones lying beneath the imperforate dorsals, and the smaller less calcified ones beneath
the perforate dorsals. The segmented appearance of the notochord is due in part to
constrictions by bands of cartilage. These bands are lateral extensions of the dorsal and
ventral arcualia (basidorsals and basiventrals) round the chordal sheath, forming bridges
that connect the dorsal and ventral cartilages from which they arise. These bridges
alternate with spaces in which the chordal sheath is naked. In the trunk region, homolo-
gous bands of cartilage occur but they are so thin that they are recognizable only in
microscopical sections.
Toward the tip of the tail the differences in the sizes of the cyclospondylous centra
gradually become lost, the constrictions becoming equal in size along with the equali-
zation in the size of the perforate and imperforate basidorsals. This stage marks a near
approach to perfection in the expression of diplospondyly.
In the extreme tip of the tail the vertebral column is a gradually tapering structure
(Text-figure 36) which remains segmented up to the very end. The arrangement of the
nerve foramina with relation to the number of dorsalia is such that Goodey characterizes
this region as “heterospondylic.”” In Heptanchus (Daniel, 1934, p. 49) the segments of
the tail are said to show “an incomplete diplospondyly” in the arches both above and
below the central column. No exception is made in regard to the extreme tip of the tail.
370 Bashford Dean Memorial Volume
Concerning the occurrence of cyclospondylous centra, Goodey (1910.1) writes
as follows:
The points at which the calcified centra occur are perhaps deserving of some mention.
It seems that they are found where there are the greatest demands made for strength. At
the anterior end, combined with the fusion of the vertebral column to the cranium, they
give a rigidity to the supporting elements which is of service no doubt in enabling the fish to
cleave the water. In the caudal region they meet the demand for increased strength caused
by the purchase which the caudal fin obtains upon the water.
It might be added that in the caudal region the cartilaginous bridges across the
lateral surfaces of the chordal sheath give greater strength to the vertebral column. On
the other hand, the diplospondylous condition gives greater flexibility (Ridewood, 1899).
In general, the vertebrae are best developed in the region that is subjected to the most
severe stresses.
We have seen that the vertebral column of Chlamydoselachus is of interest in
a number of ways. The notochord persists, in the adult, with so little modification
that it is one of the most primitive known in living sharks. The cartilaginous elements
of the vertebral column are of a very simple elasmobranch type and illustrate various
stages in the formation of complete vertebrae. In the cervical and caudal regions one
finds early stages in the formation of cyclospondylous centra; these arise as calcifications
in the chordal sheath. In the main region of the tail the dorsal and ventral arcualia are
connected by cartilaginous bridges, giving unity and completeness to the structure of
each vertebra. In the region of transition from body to tail, monospondylous vertebrae
gradually give way to diplospondylous vertebrae. Finally, at the extreme tip of the tail
there is a condition of heterospondyly which is perhaps unique among selachians.
APPENDICULAR SKELETON
The appendicular skeleton of Chlamydoselachus includes the cartilaginous frame-
work of the pectoral and pelvic fins, together with the pectoral and pelvic girdles; and
the cartilaginous supports of the dorsal and anal fins. The endoskeletal supports of the
tail fin belong mainly to the axial skeleton, but it is convenient to consider the framework
of the caudal fin along with the skeletons of the other fins.
PECTORAL FINS AND GIRDLE
The skeleton of the pectoral fin of Chlamydoselachus has been described and figured
by Garman (1885.2); Braus (1902); Deinega (1909 and 1923); and Goodey (1910.1). The
pectoral girdle or coraco-scapular (Text-figures 37 and 38) bears a decided resemblance
to that of Heptanchus (Daniel, 1934, Fig. 54); but in the fin proper the radials of Chlamy-
doselachus are relatively shorter, and are segmented to form typically three rows of
cartilaginous elements while Heptanchus has about twice that number.
Braus’s figure of the pectoral fin skeleton of Chlamydoselachus portrays a ventral
view. It differs from Garman’s figure (aspect not stated) in a number of details, as may
The Anatomy of Chlamydoselachus 371
Text-figure 37.
Pectoral girdle and endoskeleton of pectoral fin of
Chlamydoselachus, aspect not stated.
cr, coraco-scapular; msp, mesopterygium; mtp, metapterygium;
prp, propterygium.
After Garman, 1885.2, Fig. 2, pl. XI.
be seen upon comparing Text-figures 37 and 38.
There are differences in the number, sizes and shapes
of the basal cartilages, particularly the mesopterygium.
In Garman’s figure this is triangular in outline, in
Braus’s figure it is more nearly quadrangular. The
anterior radials are fused over a considerable area in
Braus’s figure, but exhibit a more limited amount
of fusion in Garman’s figure. In Braus’s specimen,
many of the radials posterior to the region of fusion
have four or five segments; in Garman’s specimen,
there are nowhere more than three segments of a
single radial. Deinega’s Fig. 14, Taf. IV, portraying
a pectoral fin (aspect not stated) of Chlamydoselachus
closely resembles Garman’s figure (my Text-figure 37)
save that right and left are reversed. Deinega’s Fig.
15, Taf. IV, representing an inner (ventral) view of
a pectoral fin of Chlamydoselachus, more nearly re-
sembles Braus’s figure (my Text-figure 38) which is
also a ventral view. The chief differences in the fig
ures thus far considered are understandable on the
assumption that Garman portrayed a dorsal view,
and that Deinega’s Fig. 14 is also a dorsal view. In Text-figure 38.
Deinega’s figures of the pectoral fin, some of the lines Ventral (inner) view of a pectoral fin
at the distal margin are so indistinct that one cannot skeleton ef Chemposelactus:
; 5 : Co, coracoid; F, foramen for blood vessel; G,
determine the exact number of cartilaginous elements; shoulder joint; ms 1, primary mesopterygium,
but in his text he states that there are three rows of ms 2, secondary mesopterygium; mt, metapter
radial segments. Goodey’s drawing (1910.1, Fig. 18, 780m: * Propteryeium; S, scapula; ‘Ss, supra
scapula; 1-4, cartilages in line with basals.
pl. XLV) of the left pectoral fin (aspect not stated) of After Braus, 1902, Fig. 1.
Siz Bashford Dean Memorial Volume
Chlamydoselachus shows a large secondary mesopterygium, as in Braus’s figure, and the
primary mesopterygium also resembles that figured by Braus. The posterior radials are
segmented to form no more than three rows of segments. At the extreme posterior ends
of the fins shown in the various figures there are individual differences.
In connection with his study of the development of paired fins, Sewertzoff (1926,
p. 547) states:
It is now generally accepted that the skeleton of the fins of the lowest cartilaginous
fishes (Chondropterygii) has developed from metamerically disposed rays, and that the basal
cartilage of the free parts of the fin, i-e., the pro-, meso-, and the metapterygium, as well as
the girdles, were formed by the concrescence or fusion of the proximal segments of these rays.
But this view may not be considered settled, and, looking over the literature of this question,
we see that many writers, who accept the theory of the [metameric] origin of the paired
fins, pass over in silence the question of the primitive structure of their skeletons or express
themselves on that subject with considerable caution.
In the pectoral fin skeletons of both Cladodus neilsoni Traquair (Text-figure 39)
and Symmorium reniforme Cope (Text-figure 40) there is only one basal that can be
Text-figure 39. Text-figure 40.
Pectoral girdles and fin skeletons of two fossil sharks, Cladodus and Symmorium.
Text-figure 39. Endoskeleton of the pectoral fin of Cladodus nielsoni Traquair.
B, basal piece; BL, fracture line; Mt, metapterygium; R, radial; S, furrow in outer proximal margin of
the metapterygium.
From Braus, 1902, Fig. 2; after Traquair, 1897, Fig. 1, pl. IV.
Text-figure 40. Fragment of a pectoral fin skeleton of Symmorium reniforme Cope.
B, basal piece; Mt., metapterygium; R, some small radials at the distal end.
From Braus, 1902, Fig. 3; after Cope, 1895, Fig. 1, pl. VIII.
The Anatomy of Chlamydoselachus 373
Text-figure 41.
Pectoral fins of the fossil sharks (A) Cladoselache, (B) Ctenacanthus, and (C) Cladodus neilsoni,
indicating the mode of origin of the metapterygial axis.
B, basalia; M, muscle of hindmost region of the fin; R, radials; SG, shoulder girdle.
After Dean, 1909, Fig. 28.
homologized with a basal in recent fishes, and it is considered to be a metapterygium.
In front of this element there is, apparently, a series of radials in direct articulation with
the pectoral girdle. In Symmorium the metapterygium itself shows a segmentation,
probably metameric, along its distal margin. If the above interpretations are correct,
they afford evidence that basals are developed by the concrescence of proximal segments
of radials. For comparison I have inserted Dean’s (1909) figures (my Text-figure 41) of
the pectoral fins of Cladoselache, Ctenacanthus and Cladodus neilsoni. The origin of the
girdles (discussed on p. 376) is obscure, but there seem to be sufficient data to warrant an
acceptance of the theory of the metameric origin of the basals of the paired fins.
PELVIC FINS AND PELVIS
Since the pelvic fins of the male Chlamydoselachus are highly modified to form copu-
latory organs (myxopterygia), it is necessary to describe the pelvic fins of the two sexes
separately.
Petvic Fins AnD Petvis OF THE FeMALE.—The pelvis and the pelvic fin skeleton of
the female Chlamydoselachus have been described and figured by Garman (1885.2),
Deinega (1909 and 1923), and Goodey (1910.1). The figures by Garman and by Goodey
are reproduced as my Text-figures 42, 43, and 89 (p. 434).
The pelvis of Chlamydoselachus, as compared with that of Heptanchus, is very long
(i.e., in the direction of the principal axis of the body). Commenting on this fact, Garman
Text-figure 42.
Dorsal view of the pelvis (one-half natural size)
of an adult female Chlamydoselachus.
bp, basipterygium; il, iliac ridge; pu, pubis.
Redrawn after Garman, 1885.2, Fig. 1, pl. XI.
374 Bashford Dean Memorial Volume
LIFT L
SOT
S 0 ° oo 68
‘ln f
Pg
Text-figure 43.
Dorsal view of the right half of the pelvis, and of the right pelvic fin, of a female
Chlamydoselachus.
btd., distal segment of the basipterygium; btp, proximal segment of the basipterygium; Inf, longitud-
inal row of foramina for nerves; pg, pelvic girdle; r, lateral radials.
Redrawn from Goodey, 1910.1, Fig. 19, pl. XLV.
(1885.2) writes: ~The peculiar shape of the pelvis suggests an embryonic character of
other sharks. In embryos the pelvis is longer than in the adult, in comparison with the
transverse measurement. An embryo of Heptabranchias before me has it half as long
as wide, proportions which are intermediate between those of the adult and an adult
Chlamydoselachus.” From another point of view one may say that an elongate pelvis
is in keeping with the general body form of Chlamydoselachus.
Textfigure 44.
Pelvic fin and girdle of the fossil shark,
Cladoselache kepleri.
b, basals; p, pelvic arch.
After Dean, 1909, Fig. 18.
Garman’s figure reproduced as my Text-figure
89 (p. 434) is a ventral view, and shows a wedge-
shaped piece inserted, at the anterior margin, between
the two paired portions of the pelvis. Thus the median
suture becomes Y-shaped. This wedge-shaped carti-
laginous element is not shown in Garman’s figure re-
produced as my Text-figure 42, which is a dorsal view
of the pelvis, presumably of the same female; nor is it
shown in any other published drawing of the pelvis of
Chlamydoselachus, male or female, dorsal or ventral.
Apparently, it is an individual variation. Deinega’s
drawing (1909, 1923) shows a median groove or suture
extending the entire length of the pelvis.
Along the lateral margins of Deinega’s drawing
of the pelvis, at regular intervals, there are faint trans-
verse grooves pierced by foramina, marking off seg-
ments in line with the radials. These transverse
grooves indicate a metameric origin of this portion of
the pelvis, presumably through the fusion of primitive
radials to form basals which were later added to the
pelvis: The manner in which basals of the pelvic fins
may be derived from radials is illustrated by Dean’s
The Anatomy of Chlamydoselachus
figure of the fossil Cladoselache (my Text-
figure 44).
In the female Chlamydoselachus, the
skeleton of the pelvic fin proper (Text-
figures 43 and 89, the latter on p. 434) is
much like that of Heptanchus as figured by
Gegenbaur (1870, Fig. 3, Taf. XV); andas
shown in my Text-figure 45a, after Daniel.
In Chlamydoselachus the basipterygium is
shorter and more of the radials are attached
directly to the pelvis. There is very little
fusion of radials in the pelvic fins of either
mn eS
i
We
Text-figure 46.
Pelvic fin skeleton of a male Chlamydoselachus:
A, viewed obliquely from above; B, viewed from
the inner (ventral) side.
Be, medial radial belonging to the myxopterygium; Bm, abdom-
inal musculature; mt, metapterygium; Mx, principal radial
of the myxopterygium; P, pelvis; R, radials; T, pocket of the
myxopterygium; TO, opening of the pocket.
After Braus, 1902, Abb. 7 and 8.
375
1a.
Text-figure 45.
Skeleton of the pelvic fin and girdle of Heptanchus
maculatus: A, female; B, male.
Be, beta cartilage; b.1—2, first and second connecting segments
ba., basal or axial cartilage; ba.p., basipterygium; pl., pelvis;
ra., radials.
After Daniel, 1934, Fig. 55.
Chlamydoselachus or Heptanchus, and this
fusion is confined to the anterior end of the
fin skeleton where some plates of cartilage
may be regarded as rudimentary basals. In
Deinega’s drawing (1909 and 1923) of the
pelvic fin of Chlamydoselachus, it is dificult
to determine the number of segments in the
radials—the row of small distal segments is
either not well shown or is absent.
Petvic Frys AND PELvis OF THE MALE.—
In the male Chlamydoselachus, the skeleton
of the pelvic fins, together with the pelvis,
has been fully described and figured by Braus
(1902) and by Goodey (1910.1). * Their figures
are reproduced as my Text-figure 46 and my
Figure 21, plate V. By comparison with
Text-figures 42, 43, and 89 (p. 434) it will
376 Bashford Dean Memorial Volume
be seen that the pelvis is alike in the two sexes. In its basal, anterior and middle portions,
the skeleton of the pelvic fin of the male is much like that of the female. In the specimen
figured by Goodey there is a slight amount of fusion of radials at the extreme anterior
end. This fusion of radials does not appear in Braus’s figure.
Osburn (1907) described and figured the pelvis and the pelvic fin skeleton of a 225-
mm. embryo of Chlamydoselachus. The sex is not stated, but the condition of the most
posterior radials is intermediate between that characteristic of the adult female and that
shown in the male figured by Braus. Osburn noted that each pelvic girdle (lateral half
of the pelvis) is pierced by eight foramina for nerves, and serves as a basal for about half
of the radials of the fin. In the mesenchyme stage, the two girdles fuse at the mid-line,
and in the stage figured “the separation at the anterior end is not yet complete.” This
“separation” presumably refers to the presence of a suture between the two cartilaginous
elements in the adult stage. In the fossil Chladoselache (according to Dean, 1909) there
are two quite separate pelvic girdles forming a pair, and in the fin skeleton the basals
consist of small rod-like elements like the radials (Text-figure 44).
After reviewing the literature on the embryological development of the paired fins
of selachians, Regan (1906.2, p. 731) states: “The mode of development of the fin-
girdles is in favor of the hypothesis that they are outgrowths of the basipterygia, and the
latter may well have been formed from the coalescence of the originally separate basal
segments of the supporting cartilages, since in the median fins also these are segmented
off from continuous laminae.” Osburn (1907, p. 188) also inclines to the view that the
origin of the girdles may be traced to the supporting elements of the fin. He compares
the pelvic girdle of Chlamydoselachus to the basals of unpaired fins.
Tue Myxoprerycta.—Posteriorly and medially, the skeleton of the pelvic fin in
the male is decidedly different from that of the female since it is enlarged and modified
to form the framework of the copulatory organ, the myxopterygium. The skeleton of the
myxopterygium or “clasper” has been described and figured separately by Gunther
(1887) and by LeighSharpe (1926), whose figures are reproduced as my Text-figures
47 and 115a (the latter on p. 472). It has also been described and figured as a part of the
pelvic fin by Braus (1902) and by Goodey (1910.1) whose figures are reproduced as my
Text-figure 46 and Figure 21, plate V. The endoskeletal elements involved in the for-
mation of this organ are in line with the basals but are in serial relation with the radials.
They appear to be radials that are enlarged, elongated and otherwise differentiated.
In the several figures, there are minor differences in the radials associated with the one
that is most highly developed, and in Braus’s specimen the skeleton of the myxopterygium
is not differentiated to the same degree as in the others. Possibly, Braus worked on
a specimen that was not fully mature. LeighSharpe’s description (1926, p. 312) of the
skeleton of the claspers, illustrated by his Fig. 54 (reproduced as my Text-figure 115a,
p- 472), is as follows:
The Anatomy of Chlamydoselachus By)
The skeleton consists of a main stout bar of supporting cartilages, the myxapterygium
[sic], with three additional minor cartilages, of which a pair on either side stiffens the apical
expansile valves, the remaining one acting as a foundation for the supposed rhipidion. Two
of the radial cartilages attached to the basipterygium, part of which is seen in the upper portion
of the figure, come down to support the walls of the clasper cavity.
Text-figure 47.
Skeleton of a clasper (myxopterygium) of Chlamydoselachus anguineus.
a, principal cartilage; a1, intermediate cartilage; b, basals of pelvic fin; 1, lobe-like expansion of cartilage a; r, 71
and r 2, rays of pelvic fin; t, tl, movable calcified terminal pieces by which the canal can be opened or closed. :
After Gunther, 1887, Figs. D and D1, pl. LXIV.
Gunther (1887) states that, as compared with other elasmobranchs, the skeleton
of the clasper of Chlamydoselachus (Text-figure 47) is extremely simple and is very similar
to that of Acanthias as figured by Gegenbaur (1870, Fig. 15, Taf. XVI). Goodey (1910.1,
p. 567) writes:
When the mixipterygium [sic] of Chlamydoselachus is compared with that of Hexanchus
griseus, described and figured by Huber, one is at once struck by the high degree of develop-
ment presented by the organ in Chlamydoselachus. Whereas in Hexanchus the axial cartilage
is represented by a comparatively short cartilage, scarcely distinguishable from a lateral
radial, and bearing no accessory cartilages; the homologous part in Chlamydoselachus is
a long, stout cartilage, furnished distally with three movable accessory cartilages.
As described by Daniel (1934) and as shown in my Text-figure 45z, the skeleton of
the myxopterygium of Heptanchus is somewhat simpler than that of Chlamydoselachus.
The skeleton of the pelvic fin of a male Raja (sp.?) figured by Gegenbaur (1870, Fig. 21,
Taf. XV]I) is simpler than any that I have mentioned. Evidently, differences in the form
of the skeleton of the claspers are of little phylogenetic significance.
THE DORSAL FIN
In the single dorsal fin of Chlamydoselachus, the cartilaginous elements (radials)
forming the endoskeleton are very irregular, as shown in my Text-figure 48. The tapering
anterior portion extends a considerable distance in front of the small membranous portion
of the fin. Garman (1885.2, p. 15) interprets this condition as follows:
378 Bashford Dean Memorial Volume
Text-figure 48.
Endoskeleton of dorsal and anal fins of Chlamydoselachus anguineus.
a, radial of dorsal fin; b, radial of anal fin; c, anterior radial of caudal fin.
After Garman, 1885.2, pl. XIII.
The great extent of the band compared with the size of the fin, and the manner in which
it dwindles toward the front, taken in connection with the fact of the continuation of the
peculiar scales of the fin-border some two inches in front of the cartilages, show that in
ancestral forms of this animal the dorsal fin was much longer, and corresponded more nearly
in proportions with the anal.
The only additional figure of the adult dorsal fin skeleton that I have found is
Deinega’s (1909 and 1923), which is reproduced as my Text-figure 49. This figure is
instructive in that it shows clearly a much greater number of cartilaginous elements
than is shown in Garman’s drawing (my Text-figure 48). Deinega distinguishes a series
of thirty-two basal elements which he calls radials, whereas in Garman’s figure there are
scarcely half as many of these elements, which he also calls radials.
Text-figure 49.
Endoskeleton of the dorsal fin of Chlamydoselachus anguineus.
m., fin membrane; 1-32, first row of radials (no. 1 not shown).
After Deinega, 1909, Fig. 12, pl. III,
The Anatomy of Chlamydoselachus 379
Osburn has published a drawing (1907, Fig. 19, pl. V) of the dorsal fin skeleton of
a 225-mm. embryo of Chlamydoselachus. The total number of cartilaginous elements
(thirty-six) is smaller than in Garman’s specimen (forty-five), and much smaller than in
Deinega’s specimen (sixty-one). The larger number in the adult may possibly be due to
fragmentation. Osburn notes the wide separation of the dorsal fin skeleton from the
axial skeleton.
In the absence of any further examples it appears that the entire endoskeleton of the
dorsal fin of Chlamydoselachus is composed of radials. Some segments of these radials
have undergone slight displacement, but there is little or no fusion. In Heptanchus
cinereus (Text-figure 50) the radials (ra.) of the dorsal fin are much more regular and there
(Z/ es
Text-figure 50. Text-figure 51.
Endoskeletons of the dorsal fins of Heptanchus and Mustelus.
Text-figure 50. Cartilages of the dorsal fin of Heptanchus cinereus.
be., basal; ra., radial cartilage.
From Daniel, 1934, Fig. 56; after Mivart, 1879, Fig. 2, pl. LXXV.
Text-figure 51. Cartilaginous elements of dorsal fin of Mustelus antarcticus.
b.c., basal segments; b.c.1, median segments; b.c.2, distal segments.
From Daniel, 1934, Fig. 89a, after Mivart.
is a large but thin basal cartilage (bc.). In Mustelus (Text-figure 51) there is a distinct
row of basal cartilages (b.c.) that appear to have been segmented off from the radials,
but there is no fusion.
There is no need of recourse to fossil forms to find evidence of the manner of origin
of basal plates in the dorsal fin skeleton. Beginning with the condition exemplified by
Mustelus, which I regard as primitive, there may be found in living forms all intermediate
conditions leading to one in which fusion of basal segments of the radials has formed
large basal plates. The literature pertaining to the fin skeletons of sharks abounds in
figures which, upon comparison, illustrate the point, but it is sufficient to cite Mivart’s
(1879) well-known drawings. In Chlamydoselachus the endoskeleton of the dorsal fin,
though primitive, seems to have suffered regression as evidenced by the irregular form
and arrangement of many of the cartilaginous elements.
380 Bashford Dean Memorial Volume
THE ANAL FIN
In the endoskeleton of the anal fin of Chlamydoselachus (Text-figures 48 and 52
after Garman and Deinega respectively) there is some fusion of proximal elements, and
even a slight amount of fusion of distal elements. The elements of the basal series are
usually oriented in a different direction from the distal elements. In the adult, this
fin skeleton is very long and slender (in an anteroposterior direction). The same is true
of the anal fin skeleton of a 225-mm. embryo figured by Osburn, 1907 (Fig. 6, pl. IV).
In this embryonic specimen the fusion of basal elements is not so pronounced. The separa-
tion of the fin skeleton from the vertebral column is very marked. In Heptanchus cinereus
(Daniel, 1934, Fig. 57 after Mivart) there is a fairly large basal element in series with
some smaller basal elements, all apparently formed by the fusion of radials.
fon
Yas: Sy
o>
aa OLIIDINL SDSS
Text-figure 52.
Endoskeleton of the anal fin of Chlamydoselachus anguineus (showing basals 1-20).
After Deinega, 1909, Fig. 13, pl. IV.
THE CAUDAL FIN
The general appearance of the cartilaginous supports for the dorsal and ventral
lobes of the greater part of the tail fin is shown in Deinega’s (1909 and 1923) Fig. 9, pl. III,
which is too large for satisfactory reproduction here; also in Garman’s (1885.2) Pl. 14,
which was drawn from a specimen in which the tip of the tail had been mutilated during
life. Details are better shown in Goodey’s (1910.1) drawings reproduced herein as
Text-figures 31 and 36.
The cartilaginous supports for the ventral lobe of the caudal fin of Chlamydosela-
chus are supplied almost entirely by the haemal spines, which belong to the axial skeleton.
The occurrence of small radials distinct from the haemal spines is confined to the anterior
portion (Text-figures 31 and 48) of the ventral lobe, and these radials are possibly seg-
mented off from the haemal spines.
The cartilaginous supports for the dorsal lobe of the caudal fin of Chlamydoselachus
consist partly of neural spines, which belong to the axial skeleton; but there is an entire
series of dorsal radial elements (Text-figures 31 and 36) distal to the neural spines.
‘For a short distance in front . . . the series is separated by a space from the neural
The Anatomy of Chlamydoselachus 381
intercalaria, as if the radials had originated, like those of the dorsal and anal [fins] in’
dependently, and afterwards through downward growth had in the greater portion of the
extent come in contact with the neural processes. These radials and interneurals are
not fused like the radials and haemapophyses” (Garman, 1885.2, p. 16). With this
interpretation Goodey (1910.1, p. 553) seems to agree, for he says: ‘The dorsal radial
supports of the caudal fin I do not consider as dorso-spinalia, because at their commence-
ment anteriorly they are not always continous with the neural arches, and, moreover,
there is as much evidence to show that in general they originate independently of the
vertebral column as there is in favor of their being portions segmented off from the dorsalia
below them.”
In the section on external characters, attention has been called to the shortness of
the cartilaginous fin rays of Chlamydoselachus, as compared with their condition in one
of the most primitive of fossil sharks, Cladoselache. We are now in a position to ask,
is there any evidence, in the patterns of the fin skeletons, to support the view that the
somewhat rudimentary character of the appendicular skeleton in Chlamydoselachus is
secondary, not primary? Along with the fusion of radials to form basals, radials are
found breaking up into segments which do not always retain their original alignment.
The shapes of these segments are sometimes irregular. As indicated by Woodward
(1921), this fragmentation and displacement of typical parts seems to indicate retro-
gression. The shortness of the radials is presumably due to arrested development.
THE MUSCULAR SYSTEM
Only the skeletal or voluntary striated muscles are considered here. Little is known
concerning smooth muscle and cardiac muscle in Chlamydoselachus, and in any case
these are best considered in connection with the organs of which they forma part. It is
convenient to classify the skeletal muscles upon an embryological basis. In Chlamy-
doselachus, as in other vertebrates, most of these muscles may be assigned to two great
groups, the metameric muscles and the branchiomeric muscles. The great muscles of the
body wall are metameric muscles. The branchiomeric muscles are of visceral-arch origin,
but they do not include all the muscles attached to the visceral skeleton.
THE METAMERIC MUSCLES
The metameric muscles of fishes are divisible into two groups: the axial muscles, in
which the metamerism is clearly expressed even in the adult; and the appendicular muscles
or fin muscles. In the latter, the metameric condition is seldom recognizable in the adult;
nevertheless, in primitive fishes the appendicular muscles arise from the metamerically
arranged myotomes of the early embryo.
382 Bashford Dean Memorial Volume
THE AXIAL MUSCLES
In fishes the axial muscles comprise (a) the great masses of muscle contributing to the
formation of the body wall and tail; (b) a group of muscles in the hypobranchial region;
and (c) the muscles that move the eyeballs.
Muscies OF THE TRUNK AND Tat.—Metamerism is such a striking feature of the
trunk muscles of fishes that it overshadows the longitudinal division into muscle bundles
or layers and the incipient differentiation into individual muscles—a development that,
in the higher vertebrates, quite reverses the picture.
Text-figure 53.
Lateral view of the body musculature in the
pectoral region of Heptanchus maculatus.
cl., gill-cleft; d.b., dorsal bundle; d.f., dermal fin rays;
d.r.m., dorsal radial muscles of pectoral fin; I.b., lateral
bundle; I]., lateral line; ms., myoseptum; tr., trapezius
muscle; v.b., ventral median muscle.
After Daniel, 1934, Fig. 90.
In surface views of the six large embryos
ot Chlamydoselachus in the American Museum,
ranging from 190 mm. to 374 mm. in length, the
myomeres are more or less sharply defined.
Along the lateral surfaces of the trunk and tail
they are clearly outlined, and in some specimens
they may be traced ventrally as far as the tropeic
folds. Dorsally, they are usually obscure and in
this situation better views were obtained by
removing patches of skin from one of these em-
bryonic specimens. In the adult specimens, only
Slight indications of the body musculature could
be seen until after the skin had been reflected:
then the myosepta stood out boldly. It is ap-
parent, even from a cursory study of our mate-
rial, that the myomeres of the trunk region of
Chlamydoselachus conform to the primitive
elasmobranch type and bear a close resemblance
to those of Heptanchus as described and figured
by Maurer (1912) and Daniel (1934). From
Daniel (1934, p. 89) I quote the following para-
graph which is illustrated by my Text-figure 53:
Ina side view, the muscles of the body of Heptanchus maculatus are divided at the lateral
line (J].) into dorsal bundles (d.b.) which attach to the cranium, and ventrolateral bundles
which attach to the pectoral girdle. Both the dorsal and the ventrolateral muscles extend
to the tip of the tail. In these bundles the myosepta (ms.) are bent into zigzag shape. Above
the lateral line one of the columns has the apices of its myosepta directed forward, the other
backward. Below the line there appears to be a single column with apex pointed posteriorly.
Some of the anterior fibers of the ventral bundle are specialized as the pectoral muscles of
the pectoral fin.
Howell (1933, p. 249) attaches considerable significance, from a developmental
point of view, to the longitudinal division of the trunk musculature of fishes into dorsal
and ventrolateral bundles. His account of the developmental processes leading to this
condition follows:
The Anatomy of Chlamydoselachus 383
A frequent misconception regarding the development of the musculature is to the
effect that the muscles ventral to the lateral line are formed by actual growth in that direction
of the original, dorsally situated myotomes. Conditions vary in different parts of the body,
but in the anterior trunk at least there appears to be a lateroventral muscle mass entirely
distinct from the dorsal myotome. Between the two there is a connective tissue septum,
and tending further to separate them at early stages of phylogeny are the pronephros and its
duct, and the lateral line structures. The lateroventral musculature differentiates by con
densations of mesoderm progressively in a ventral direction, forming a lateral somatopleure,
giving rise to the somatic musculature, and a medial splanchnopleure, from which is derived the
smooth musculature of the intestinal tract. Whether or not all the striated branchial muscles
are also derived from this element is not entirely certain. Between the two plates is a coelomic
cavity. In other parts of the body, or in vertebrates that have long since discarded all vestige
of a lateral line system, the distinctiveness in origin of the dorsal from the lateroventral
musculature tends to become obscured in the embryonic picture.
DORS.
a ——_ ee
Text-figure 54. MUSS PN
Model of myomere of a selachian A
(Squalus), showing divisions into LAT. LINE. --
longitudinal muscle bundles.
DORS.MUSC.DIV., dorsal bundle; LAT.
LINE, lateral line; LAT.M.DIV., lateral
bundle; VENT.M.DIV., ventral bundle.
After Howell, 1933, Fig. 3, modified from
Langelaan and Daniel.
--- LAT. M. DIV.
VENT. M. DIV---->
EE
A model of a single myomere of the trunk region of a selachian is illustrated by
Text-figure 54. Regarding the basic segmental features of vertebrate trunk musculature,
Howell (1933, pp. 255-256) writes:
The original plan of vertebrate trunk musculature, well illustrated by cyclostomes,
involves a series of segmental muscles each of which is separated from the muscles of adjoining
segments by myocommata or myosepta. The axially directed muscle fibers of each segment
are basically divided into a dorsal division, above the lateral line on either side of the mid-line,
and a continuous lateroventral division below; this constitutes the primary muscular plan.
It is a primitive scheme, suited to a low vertebrate that can bend with equal facility in any
direction—the essentially vermiform type of control.
In this plan the myosepta are virtually transverse and usually gently curved. Unlike
the situation in mammals, most of whose muscles have one end solidly anchored on bone, in
the primitive state the fibers at both ends are attached to yielding connective tissue. Accord-
ingly there was originally a tendency for some of the groups of fibers to pull certain parts of
the myosepta in a forward and others in a backward direction, as a result of specialized action
of the groups concerned. This would have a contortional effect upon the myosepta, and in
consequence some parts would have an anterior and others a posterior inclination, as suggested
in the given diagram of a myomere of a shark (Fig. 3) [Text-figure 54 herein]. Presumably
the swifter the fish (i.e., the stronger the muscle action) the more tortuous the pattern of
the myosepta.
384 Bashford Dean Memorial Volume
sS==
\\
AK
SS}
Text-figure 55.
Lateral view of the trunk musculature of Chlamydoselachus in four different regions: A, anterior part of the
trunk; B, middle part; C, posterior part; and D, anterior portion of the tail.
a, b, c, d, the four longitudinal divisions of the ventral bundle (ventrolateral of other authors); al (alpha), be (beta), and ga (gamma),
the three longitudinal regions into which the division b may be divided; I, lateral line; o. inf., musculus obliquus inferior; o.s., musculus
obliquus superior; R.p., rectus profundus muscle—in A it is shown artificially spread out, as well as in its original position, inrolled.
A line drawn from ~x to y, along each region, would separate, approximately, the inferior oblique from the superior oblique muscles.
After Maurer, 1912, Fig. 1, Taf. 1.
Maurer (1912) has given us detailed information concerning the trunk musculature
of both Chlamydoselachus and Heptanchus. In Chlamydoselachus (Text-figure 55) the
ventrolateral bundle has the same fundamental division into two columns (divided
otherwise by Maurer) as is found in the dorsal bundle. This is best exemplified in the
region of the base of the tail (Text-figure 55p) where the ventrolateral bundle is the
SS
===>
SS
= —
A
ae 0. ing
Text-figure 56.
Lateral view of the trunk musculature of Heptanchus cinereus.
a., dorsal region of ventral bundle (ventrolateral of other authors); d., dorsal bundle; I., lateral line; o.inf., inferior
oblique; 0.m. x0.s.. portions of middle oblique and superior oblique overlapped by inferior oblique; o.s., superior
oblique; S, shoulder girdle.
After Maurer, 1912, Fig. 4, Taf. 2.
The Anatomy of Chlamydoselachus 385
mirrored image of the dorsal bundle; but it is expressed, with some modifications, in the
trunk region also. These modifications have to do with (a) the incipient separation of
a superior oblique muscle from an inferior oblique, and (b) the inrolling of the ventral
column of the ventrolateral bundle to form the muscles of the tropeic folds—structures
peculiar to Chlamydoselachus. In Heptanchus (Text-figure 56) conditions are not so
simple, for there is a small middle oblique muscle and there is considerable overlapping
of the middle and superior oblique muscles by the inferior oblique. The figure for Chlamy-
doselachus is drawn from a rather small specimen, 1330 mm. long. The figure for Heptan-
chus is from a specimen 900 mm. long.
Since the abdominal or tropeic folds are structures peculiar to Chlamydoselachus,
their musculature is entitled to further consideration. The superficial appearance of the
tropeic folds has been described, in three adult specimens and six large embryos, by
Text-figure 57.
Transverse section showing the tropeic
folds (x 1) of an adult Chlamydo-
selachus. This section was taken eight
inches in front of the pelvis.
After Garman, 1885.2, Fig. B, pl. XX.
Gudger and Smith (1933). The internal structure of the abdominal folds in a single
adult specimen has been figured by Garman (1885.2) in his Figs. A and B, pl. XX—the
latter figure being reproduced as my Text-figure 57. Concerning these figures Garman
(p. 21) says:
One of the folds is seen to hang below each of the large abdominal vessels. The vessels
are parallel or nearly so. Between them are two muscular bands, one to each fold. Each
band is nearly an inch in width, very thin at its lower edge, and near one-fifth of an inch thick
toward the rounded upper edge, between the veins. The fiber in these tropeic . . . or keel
muscles differs from that in the walls of the flank in being coarser in the bundles and plates,
and more loosely put together. Apparently the keel muscle corresponds to the rectus
abdominis of lower vertebrates.
Garman’s figures readily suggest that the keel muscle is derived during development
by an infolding of the musculature of the ventral body wall. In order to test this hypoth-
esis I have prepared transverse serial sections from a segment of the ventral abdominal
wall excised from a 210mm. male embryo. In this specimen the distance from pectoral
fin to pelvic girdle is 55 mm. The segment comprised the region extending from 10 mm.
to 20 mm. in front of the pelvic fins. A drawing (Text-figure 58) was made from a section
taken approximately 15 mm. from the pelvic fins—corresponding very nearly to the region
(200 mm. in front of the pelvic girdle) figured by Garman for his large adult specimen.
In my sections I have found some further indications of the manner of origin of the muscle
386 Bashford Dean Memorial Volume
Text-figure 58.
Section through the tropeic folds (x 25) of a 210 mm. embryo of Chlamydoselachus, showing
the keel muscle (k.m.). The section was taken about 15 mm. in front of the pelvis.
Drawn from a specimen collected in Japan by Dr. Bashford Dean, and now in the American Museum.
under consideration. It is clearly derived as a simple inpocketing of the ventral muscula-
ture of the body wall, in the region where the ventral bundles of the two sides of the
body meet. Furthermore, it is segmented after the fashion of the metameric muscles of
the body wall—a feature that is entirely lacking in Garman’s drawings and is not men-
tioned in his text. Earlier stages would be required to show continuity of the muscula-
ture in this region.
Evidence regarding the manner of origin of the keel muscle was obtained by Braus
(1898, Fig. 2, pl. XIII) in connection with his studies of the innervation. In this case
the depth of the “keel” is remarkable. Braus applies the term rectus to the thin muscle
of the body wall in the region of the ventral mid-line—a muscle which is interrupted by
Ke
i Lil --Per
H i ONG Ain ahr
ute. B NG
ie perio
Mobl int x A
N. intercost.
Text-figure 59.
Diagrams of sections (all inverted) showing the probable manner of origin of the keel muscle:
A, absent in Squalus; B, hypothetical intermediate stage; C, as in adult Chlamydoselachus.
H. skin; M.obl.int., musculus obliquus internus; N.i., intercostal nerve; Per., peritoneum;V.p., vena parietalis,
After Braus, 1898, Text-fig. 3.
The Anatomy of Chlamydoselachus 387
the tropeic groove. The deep muscle that Garman calls the rectus abdominis or keel
muscle is called by Braus simply the keel muscle. Braus (1898, p. 337) states that the
nerves that innervate the keel muscle lie on its lateral surface, and not on the medial
surface as in the case of the musculus rectus abdominis and the oblique muscles of the
body wall. He concludes, therefore, that an invagination, leading to inversion, of the
ventral body wall has occurred at the mid-line; for it is well known that nerves ending in
developing muscles tend to follow these muscles in their migrations. Braus has embodied
these conclusions regarding the phylogenetic origin of this muscle in a diagram which
I have reproduced as Text-figure 59.
Text-figure 60. Text-figure 61.
Transverse sections of the ventral body wall of Chlamydoselachus showing the inrolling of the
musculature in the region of the tropeic folds.
Text-figure 60. Transverse section of the ventral abdominal wall immediately behind the
pectoral girdle.
la., linea alba; P., peritoneum; o.inf., musculus obliquus inferior; R.p., rectus profundus muscle, which is recognizable
as an inrolled portion of the ordinary musculature of the body wall.
After Maurer, 1912, Text-fig. 1.
Text-figure 61. Diagrams showing the condition of the ventral musculature on one side of the
body in four different regions: A, just behind the pectoral and likewise immediately in front
of the pelvic girdle; B, in the second quarter, and C, in the third quarter of the trunk.
R.p., musculus rectus profundus; a, first; and b, second fold of the rectus profundus.
After Maurer, 1912, Text-fig. 3.
Maurer (1912) has given a somewhat different picture (Text-figures 60 and 61) of
the manner of origin of the deeply situated ventral longitudinal muscle, which he calls
the rectus profundus. These figures are based on sections taken from four different
regions along the ventral body wall of his adult, or nearly adult, specimen. A connection
between the rectus profundus and the ventrolateral bundle persists in the region im-
mediately behind the pectoral girdle and immediately in front of the pelvic girdle, but
is lost throughout the remaining extent of the tropeic folds. A curious feature of all
Maurer’s drawings of the ventral musculature of his specimens is that in none of them
does he show any ventral protrusion of the body wall to form the keel which has been
described by Garman (1885.2), Collett (1897), Braus (1898), and by Gudger and Smith
(1933). But the most remarkable thing about Maurer’s drawings of the musculature of
the tropeic folds is that he represents the infolding process not as a simple invagination
but as a parting of the musculature of the body wall along the mid-line, after which each
edge becomes inrolled independently, like a scroll (Text-figures 55, 60 and 61). This
388 Bashford Dean Memorial Volume
does not accord with the conditions portrayed by other authors in their drawings of
transverse sections through the keel muscle.
As to the function of the deep muscle variously called the keel muscle, the rectus
abdominis, and the rectus profundus, it clearly aids in a rapid ventral flexion of the body;
but why it should be so uniquely set apart from the remaining musculature of the ventral
body wall is problematical.
Text-figure 62.
Diagram showing the relation between head somites and body somites, and the origin of the
hypobranchial or hypoglossal musculature from trunk myotomes, in a larval Squalus acan-
thias. The somites that degenerate in ontogeny are indicated by broken lines. The anlagen
of the six eye muscles, which arise from the first three somites, are already differentiated.
1d, dorsal moiety of the first myotome; Iv, ventral moiety of the first myotome; 2d, 2v, dorsal and ventral moieties
of the second myotome; 3v, ventral moiety of the third myotome; 7, seventh myotome; a., anterior cavities;
hyp.m., hypoglossal musculature; M., mouth; ot, otic capsule; sp., spiracle; thr., thyroid.
After Neal, 1918, Fig. 19.
Goodey (1910.1) studied the relations of the myomeres to neuromeres in the tail
and posterior part of the trunk of Chlamydoselachus. In the trunk, he found the limits
of a myomere corresponding in extent with a monospondylous neuromere. In the main
caudal region each myomere is equal in extent with a diplospondylous neuromere. In
the tip of the tail each irregularly divided or heterospondylous neuromere has its myomere.
Thus the myomeres of the tail region are not particularly influenced by the secondary
segmentation of the vertebral column in this region.
Tue HypopraANcHIAL Group.—lIn fishes, as in other vertebrates, the hypobranchial
region has a group of muscles that appear to be a continuation of the longitudinal muscula-
ture of the ventral body wall. The muscles of the hypobranchial group are attached
posteriorly to the shoulder girdle and anteriorly to ventral portions of the visceral skeleton.
This hypobranchial or hypoglossal musculature does in fact arise (Text-fgure 62, hyp.m.)
as a forward prolongation of some myotomes of the occipital and anterior trunk region
which are in strict serial relationship with the myotomes that give rise to the segmental
The Anatomy of Chlamydoselachus 389
muscles of the body and tail—as in Scyllium (Van Wijhe, 1883, p. 36 and Fig. 25, Taf.
III); in Lacerta (Corning, 1895); in Petromyzon and Squalus (Neal, 1897); and in Lepido-
siren and Protopterus (Agar, 1907).
Text-figure 63.
Hypobranchial muscles of the notidanid,
Heptanchus maculatus, ventral view.
bh., basihyoid cartilage; c.ar., musculus coracoar-
cuales; cb.1, first ceratobranchial cartilage; c.br.1-7,
first to seventh coracobranchial muscles; ch.,
ceratohyoid cartilage; c.hy., musculus coracohyoi-
deus; co., coracoid cartilage; c.md., musculus cora-
comandibularis; ibv.1-6, first to sixth ventral
interbranchial muscles; md., mandibular cartilage.
After Davidson, 1918, Fig. 4.
In Heptanchus (Davidson, 1918) the following
muscles (Text-figure 63) are recognized as members
of the hypobranchial group: the paired coracoarcu-
ales communes (c.ar.), the unpaired coracomandib-
ularis (c.md.), the paired coracohyoidei (c.hy.), and
seven pairs of coracobranchiales (c.br.1—7). In elas-
mobranchs generally, according to Daniel (1934, p.
108), all of these muscles excepting the coraco-
branchiales arise from the first five trunk myotomes.
Edgeworth (1903) states that in Scyllium the coraco-
branchiales develop from head myotomes. In the
adult Heptanchus, the metameric nature of the cora-
coarcuales is attested by the presence of a series of
four transverse or slightly oblique myosepta (Text-
figure 63). In the coracoarcuales of Scymnus, there
are five such myosepta (Furbringer, 1897, Fig. 3,
Taf. VI). In Heptanchus, Vetter (1874, Fig. 9, pl.
XV) shows a myoseptum in the coracohyoideus
muscle also.
The hypobranchial group of muscles is often
called the hypoglossal musculature because the mus-
cles of this group are supplied, somewhat indirectly,
by a nerve which, variously called the spino-occipi
tal, occipital or hypoglossal nerve in fishes and am-
phibians, in the higher vertebrates is known as the
hypoglossal (hypoglossus) or twelfth cranial nerve.
This nerve is a composite structure, made up from
a series of roots representing, perhaps, several
neuromeres.
Allis (1917 and 1923) does not distinguish the
hypobranchial muscles of Chlamydoselachus as a
separate group. However, he describes the distribution of the branches of “a large
nerve which was not traced upward to its origin, but which is either of spinal, or spinal
and occipital origin’ (Allis, 1923, p. 195). The muscles supplied by this nerve are
identical with those included in Davidson’s list of hypobranchial muscles in Heptan-
chus, with the addition of a muscle which Allis calls the “‘pharyngo-clavicularis.” The
hypobranchial muscles of Chlamydoselachus are shown, in color, by Allis (1923) in his
Figs. 35 and 37-40, pls. XIII-XV; but nowhere are these muscles of Chlamydoselachus
390 Bashford Dean Memorial Volume
figured as a complete and separate group. The coracoarcuales and coracobranchiales
muscles of one side of the head are shown in Text-figure 64 after Gregory, and the
first pair of coracobranchiales (cb.1) are shown in my Figure 8, plate HI. Allis (1923,
pp. 192-195) gives a detailed description of each of the muscles under consideration.
idhy add’id’ ad. arc’ ti Yeo oS
(TURES
lev: lab. Sup.
/ y
proangor lab.cart.
Text-figure 64.
Skull and visceral arches of Chlamydoselachus with the deep muscles of the branchiocranium. These
muscles fall into two main groups: extensors of the oral and branchial arches, running anteroposte-
riorly; and flexors, running vertically.
ad.arc., musculi adductores arcuales 1-6. ad.d., musculiadductores dorsales 1-5; ad.mand., musculus adductor mandibulae;
carc., musculus coracoarcualis; cb., musculi coracobranchiales 1-6; co.sc., coracoscapular arch; hyom., hyomandibular; id.,
musculi interdorsales 1-5; id.hy., interarcualis between hyal and first branchial arch; lab.cart., labial cartilages; lev.lab.sup.,
musculus levator labii superioris; lev.mx.sup., musculus levator maxillae superioris; pal.qu., palatoquadrate; pro.ang.or.,
musculus protractor anguli oris; trpz., musculus trapezius.
After Gregory, 1933, Fig. 4.
As one would expect from the similarity of their cartilaginous branchial frame-
works, there is a marked likeness between the hypobranchial musculatures of Chlamy-
doselachus and Heptanchus. Only a few points call for special consideration here.
There are, to be sure, only six pairs of coracobranchiales in Chlamydoselachus, as
compared with seven in Heptanchus, but this difference is correlated with the number
of gill arches. Of these muscles in Chlamydoselachus, Allis (1923) says: “The more
posterior coracobranchiales have no connection whatever with the musculi coraco-
arcuales, Chlamydoselachus differing markedly in this respect from Heptanchus (Vetter,
1874) and closely resembling Acanthias (Vetter, l.c.)." In Vetter’s figure of Heptanchus
(his Fig. 9, pl. XV), the coracobranchiales of the region under consideration appear to
arise directly from the musculi coracoarcuales, while one gets a somewhat different
impression from Davidson’s figure reproduced as my Text-figure 63. Davidson (1918,
p. 162) describes the origin of the coracobranchiales muscles of Heptanchus as follows:
The Anatomy of Chlamydoselachus 391
The first [coracobranchialis muscle] has its origin in the connective tissue directly over
and attached to the coracohyoideus muscles. The origins of the second to the sixth coraco-
branchiales are in the strong connective tissue just dorsal to the coracoarcuales. The anterior
part of the origin of the seventh is continuous with the origin of the sixth while the posterior
part has its origin on the pectoral girdle, just lateral to the origin of the coracoarcuales.
Until we know more of the relations of the sheet of connective tissue that affords
origin to the coracobranchiales of Heptanchus we cannot be sure that these muscles
have any real connection with the coracoarcuales. Comparison should be made directly
from dissections of the two forms.
The muscle which Allis calls the pharyngo-clavicularis is described by him (1893,
p. 195) as follows:
Immediately dorsoposterior to the surface of insertion of the coracobranchialis VI on
the sixth ceratobranchial, a broad muscle has its origin, and running ventromesially and
contracting rapidly has its insertion on the clavicle dorsolateral to the coracoarcualis muscle
of its side. This muscle would seem to be the homologue of the pharyngo-clavicularis of
Amia (Allis, 1897), and it is not described by Vetter as a separate muscle in any of the
selachians considered by him.
Tue Eyzsatt Grour.—In elasmobranchs and perhaps in vertebrates generally,
the muscles that move the eyeballs arise (Marshall, 1881; Van Wijhe, 1883; Neal, 1918)
M. oblig. sup.
™. rect lat.
Verbindung des
Kiemenbogen-
coeloms mit dem
Cavum pericardii
Text-figure 65.
Diagrams showing the origin of eye muscles, and the extensions of the primitive coelomic
cavity into the gill-arches, in selachian embryos. In A, the cavities of the pharyngeal
arches are shown communicating with the pericardial portion of the coelomic cavity; in B,
which is a later stage, the connections of these cavities have been lost.
1, 2, 3, 4, gill-clefts; S.B.C.1—5, pharyngeal arch extensions of the coelomic cavity; ch.dors., chorda dorsalis;
oc.m., anlagen of the oculomotor muscles; M. oblig. sup. and M.rect.lat., anlagen of the superior oblique and lateral
rectus muscles respectively; ves.audit., otic vesicle.
After Corning, 1925, Figs. 222 and 223; based on Froriep’s (1902) Figs. 4 and 5 (Torpedo ocellatus).
392 Bashford Dean Memorial Volume
from mesodermal segments (head somites) which are serially homologous with those of
the trunk (Text-figure 62). In primitive fishes, the head somites, like the trunk somites
of vertebrates generally, are at first hollow and their cavities communicate with the
primitive coelomic cavity. In other words, the coelomic cavity extends into the somites.
In the head, this communication is by way of the mesoderm of the branchial arches,
as shown (for Torpedo) in Text-figure 65 after Corning. Van Wijhe (1883, Figs. 1 and 2,
Taf. I) gives more exact drawings showing the same features in Scyllium canicula. These
channels quickly close, and the somites later become solid structures.
Text-figure 66.
Dorsal view of the eye muscles of Chlamydoselachus on the right side.
The Roman numerals distinguish the nerves supplying the eye: II, second cranial or optic nerve; III, third
cranial or oculomotor nerve; IV, fourth cranial or trochlear nerve. Other abbreviations are self-explanatory.
After Nishi, 1923, Fig. 1.
In Chlamydoselachus, the muscles of the eyeball and their innervation were described
from two specimens by Hawkes (1906), and later by Nishi (1922) who used four adult
specimens. They were considered briefly by Allis (1923), who merely supplemented the
work of Hawkes by comparisons with his own specimens.
The disposition of the various eye muscles of Chlamydoselachus is shown in Figures
10, 11, and 12, Plate IV; also in Text-figures 66 and 67. It will be seen from Text-figure 67
that the dorsal side of the eyeball has three muscles, while only two muscles supply the
The Anatomy of Chlamydoselachus 393
ventral side. The combined strength of the dorsal group is obviously greater than that
of the ventral group. As figured and described by Hawkes the inequality in the strength
of these two groups is more striking. The dorsal group is strengthened to turn the eye
upward, not only to a moderate degree for the purpose of looking upward, but to a much
greater extent when the cornea is turned well under cover of the socket, for protecting
this most delicate part of the surface of the eyeball. The part of the eyeball (sclera)
then left exposed is covered with shagreen. These devices for protecting the eyes in
the absence of lids have been described by Gudger and Smith (1933).
Conditions are simpler in Heptanchus as described and figured by Davidson (1918,
pp. 162-163 and Fig. 5). In this shark two groups of muscles (Text-figure 68) are present
in the orbit. The first group is placed anteriorly and consists of the superior oblique
Rect b PSs
ectus sup. snd ie Obliquus sup.
Rectus lat. acc. ~-...../
_- Rectus med.
Rectus lat. ate
ot bceeS N. ophthalm.
prof.
“ss. N. opticus.
Rectus inf. ol AN kf SSS Obliquus inf.
Text-figure 67. Text-figure 68.
Eye muscles of Chlamydoselachus and Heptanchus showing insertions on eyeballs.
Text-figure 67. Semidiagrammatic figure of left bulbus oculi of Chlamydoselachus
in medial aspect.
The abbreviations are self-explanatory.
After Nishi, 1923, Fig. 2.
Text-figure 68. Eye muscles of Heptanchus maculatus in dorsal view, right side.
a.r., anterior rectus; i.o., inferior oblique; i.7., inferior rectus; n.II, optic nerve; o.p., optic pedicel;
p.r., posterior rectus; S.0., superior oblique; S:T5 superior rectus.
After Davidson, 1918, Fig. 5.
(s.o.) and the inferior oblique (i.o.). These muscles extend from the anterior part of the
orbit outward and caudad to be inserted on the eyeball. The second group consists of
the four recti muscles, all of which arise from the posterior surface of the orbit around
the base of the optic pedicel. The most dorsal member of this group is the superior rectus,
the most ventral the inferior rectus, the most posterior the external or lateral rectus, and
the most anterior the internal or medial rectus. They pass outward and forward to be
inserted on the eyeball.
The chief peculiarity of the musculature of the eyeball of Chlamydoselachus 1s
the fact that all the musculi recti, save only a portion of an accessory rectus lateralis
(externus), take origin from the eyestalk. In Chlamydoselachus the function of the eye-
394 Bashford Dean Memorial Volume
stalk is twofold: it prevents the eye from sinking too far into the socket, and it supplies
a more lateral basis for the origin of the recti muscles. The lateral rectus consists of two
parts which have separate origins and insertions, although they are otherwise united by
strong strands of muscle fibers. One division of this muscle takes origin from the outer
part of the optic stalk, while its insertion is on the posterior surface of the eyeball. This
is the normal insertion for an undivided rectus lateralis. The other division is said by
Hawkes to be twice as large, though in Nishi’s figures (reproduced here as Text-figures
66 and 67) it appears slightly smaller than it does in Hawkes’ figures. Its origin is from
the cranium as well as along the proximal! portion of the optic stalk. The insertion is on
the dorsal side of the eyeball, somewhat more external than that of the rectus superior
which it partly overlaps. From the positions of its origin and insertion, this division
must be considered as a secondary or derivative portion of the primitive rectus lateralis.
This secondary muscle was probably split off from a typical rectus lateralis to aid the
superior rectus and the superior oblique in tilting the eye upward. The recti superior,
medialis (internus) and inferior are all attached to the top of the optic stalk, just below its
flattened head.
THE APPENDICULAR MUSCLES
From embryological studies on certain elasmobranchs and primitive teleostomes it
is clear that, in these fishes, buds from the myotomes grow into the embryonic fins and
there break down into mesenchyme which is the source of the fin muscle: as in Spinax
(Braus, 1899); Scyllium (Goodrich, 1906); Cestracion (Osburn, 1907); Acanthias (E.
Muller, 1911); in Amia and Lepidosteus (Schmalhausen, 1912). Thus the muscles that
move the fins are metameric in origin; this applies to both paired and unpaired fins.
Some features of this developmental history have been interpreted in terms of the fin-fold
theory of the origin of paired fins. Concerning this matter, Daniel (1934, p. 110) says:
It is evident that the number of segments that take part in the formation of buds for the
pectoral fin is fewer in the sharks than in the rays. This fact is clear when we consider two
types like Mustelus and Torpedo, in the former of which the fin is relatively narrow and in
the latter is of great extent. According to Maurer (1912), in the embryo of Mustelus only
10 segments contribute to the formation of the musculature of the pectoral fin; while in
Torpedo there are 26 such segments.
The further course of the development of these buds in two forms like the above has been
studied in great detail because of the bearing which such development has on the lateral
fin-fold theory. That, in a type like Mustelus, segments (myotomes) anterior to the pectoral
fin and between the pectoral and the pelvic fins form buds which atrophy without entering the
fin, is taken by those who accept the lateral fin-fold theory to mean that the fin previously
had a much greater anteroposterior extent than at present; and it is hence in agreement with
what would be expected from that theory.
In common with the notidanids, Chlamydoselachus seems to afford favorable material
for the study of the origin and development of the fin muscles, but so far as ] am aware,
such studies have never been made on these forms.
Of the fins of Chlamydoselachus, only the pelvics of the male have received attention
with respect to their musculature. The muscles of these fins have been described in
The Anatomy of Chlamydoselachus 395
Text-figure 69.
Endoskeleton and musculature of male pelvic fins of
Heptanchus maculatus.
A—Skeleton of male left pelvic fin in dorsal view.
b.1 and b.2, connecting segments; ba., basal piece; ba.p., basipter-
ygium; be., beta cartilage: pl., pelvic girdle; ra., radial cartilages.
After Davidson, 1918, Fig. 8.
B—Musculature of male right pelvic fin in dorsal view.
ad., adductor muscle; cb., compressor muscle; dl., dilator muscle;
f.e., flexor externus; f.i., flexor internus; pl., pelvic girdle; ra., radial
muscles; s.m., muscle of sac or pocket.
After Davidson, 1918, Fig. 9.
detail by Goodey (1910. 1, pp. 564-565) whose
Figs. 20 and 21, pl. XLVI, are reproduced as
my Figures 22 and 23, plate V, alongside Fig-
ure 21 which shows the endoskeleton. The
radial muscles (Ra., Figure 23, plate V) ex-
hibit a division into bundles paralleling the
radial cartilages. Concerning the ventral radial
muscles Goodey says: “‘On the ventral side
there are the radial muscles Ra., which originate on the pelvic girdle close to the
median line and extend outward to the horny fibers. Toward the anterior end the separate
bundles have fused together, thus corresponding with the fusion of the radials above.”
The muscles of the clasper have been described in Heptanchus by Davidson (1918,
pp. 165-167 and Fig. 9). Davidson’s figure of the musculature is here reproduced as
Text-figure 69B alongside his figure of the endoskeleton (Text-figure 69a). In both
Chlamydoselachus (Figures 22 and 23, plate V) and Heptanchus (Text-figure 69s), the
musculature of the myxopterygium is simple as compared with that of most elasmobranchs.
Few differences are found when Chlamydoselachus and Heptanchus are compared with
each other. As pointed out by Daniel (1934, p. 110), the principal difference is in the ad-
ductors. In Heptanchus the adductor (ad. in Text-figure 69s) is a long muscle; in Chlamy-
doselachus it (A in Figure 22, plate V) is relatively broad and fan-shaped. Also, in
Heptanchus the external and internal flexors are united at their origins, while in Chlamy-
doselachus the point of origin of the external flexor is far removed from that of the
internal flexor.
From a functional point of view, certain muscles of the myxopterygia or claspers
of Chlamydoselachus are described by LeighSharpe (1926, p. 312) as follows: ‘The
musculature is represented by the anteroflexor muscle, which anteroflexes the whole
clasper for intromission, and the erector muscle which in this case causes expansion of
the apical valves by pulling on a common tendon. The anteroflexor muscle is strongly
developed in this genus.’ These muscles are shown (p. 472) in Text-figure 115s, after
LeighSharpe.
396 Bashford Dean Memorial Volume
THE BRANCHIOMERIC MUSCLES
The segmentation that gives rise to the branchial arches is of a different nature from
that which carves out the somites. The term branchial arches is used by embryologists,
in its widest sense, to include the mandibular and hyoid arches which are considered
to be modified gill arches. By comparative anatomists, the entire series is usually designat-
ed the visceral skeleton, and the arches are called visceral arches. It is common to speak
of the branchiomeric muscles as the pharyngeal muscles, here also making no distinction
between mouth and pharynx.
supemicial constrictor
iby muscles of Gillarthes
Mm
RheTVe
Spiracte
W\\S RQ \
SX \\
QO SEERA
S
= eM ey
ZA
lalla el
CUMS pity adductor muscles
cartilage OF ja WS
Text-figure 70.
A dissected head of Chlamydoselachus anguineus in lateral view.
From Gregory, 1933, Fig. 6; redrawn and slightly simplified after color figure in Allis, 1923, pl. IV.
While the metameric muscles are derived, at least in large part, from a dorsal zone
of early mesoderm which has previously been cut up into somites, the muscles of the
branchial (visceral) arches (excluding the hypobranchial group of muscles) do not arise
from somites but from mesoderm that is commonly regarded as splanchnic. The nerves
that supply these muscles are placed in a different category (visceral) from those (somatic)
that supply metameric muscles.
Furbringer (1903) described some of the muscles of gillarch origin, particularly
those of the mandibular arch, in Chlamydoselachus. Luther (1909) described the muscles
innervated by the trigeminal nerve. Goodey (1910.1) described the muscles of the
mandibular and hyoid arches. Allis (1923) has given a detailed, comprehensive and
beautifully illustrated description of the pharyngeal muscles of Chlamydoselachus, which
The Anatomy of Chlamydoselachus 397
should be consulted by anyone wishing a more complete account than is given here.
Most of the pharyngeal muscles are represented in Text-figures 64 and 70 after Gregory
(1933). The interarcuales dorsales (Iad.) and subspinales (S.sp.) are shown in Text-figure
71, after Allis (1915), drawn from a specimen in which the interarcuales are somewhat
atypical. In Text-figures 64 and 71 the methods of numbering the interarcuales differ,
so that Allis’s interarcualis IV corresponds to Gregory’s interdorsalis V.
Text-figure 71.
Ventral view of the roof of the pharyngeal
cavity of Chlamydoselachus, after the lining mem-
brane has been removed, showing the pharyngo-
branchial cartilages, efferent arteries and inter-
arcuales dorsales muscles in natural position.
cc, common carotid artery; Coe, constrictor of the esophagus;
eal, efferent branchial artery of the first branchial arch;
eall, efferent branchial artery of the second branchial arch;
EBII, epibranchial cartilage of the second branchial arch;
EPB VI, epi-pharyngobranchial cartilage of sixth branchial
arch; HMD, hyomandibular cartilage; Iad IV, musculus
interarcualis dorsalis between arches [V—V; I adhy, musculus
interarcualis dorsalis between hyoid and first visceral arches;
Ida, lateral dorsal aorta; Imh, ligamentum mandibula-
hyoideum; n., cut ends of nerves to tissues of roof of branchial
chamber; PBI, pharyngobranchial cartilage of first branchial
arch; PBIV, pharyngobranchial cartilage of the fourth
branchial arch; Rabd, musculus retractor arcuum branchialium
dorsalis; Ssp, subspinalis muscle; tiad, ligamentous sheet
formed by tendons of musculi interarcuales dorsales.
After Allis, 1915, Fig. 1.
Davidson (1918) classified the pharyngeal (branchiomeric) muscles of Heptanchus
as follows: (1) superficial circular [constrictor] muscles; (2) interarcuales; (3) subspinales;
(4) adductors; and (5) the hypobranchials. For reasons concerned with the mode of
development, the hypobranchials have already been considered under the category
of metameric muscles, though it is more common to include them with the pharyngeal
group, to which they functionally belong.
All observers agree that the adductor mandibulae of Chlamydoselachus is “a thick
massive muscle, filling up the concavities on the outer side of the palatoquadrate and the
mandible” (Goodey, 1910.1, p. 547). In all the illustrations (by various authors) of this
398 Bashford Dean Memorial Volume
muscle, it appears surprisingly large considering the slenderness and flexibility of the
jaws. This is well shown in Gregory’s drawing (Text-figure 64 herein) and is perhaps
exaggerated in Furbringer’s (1903) Fig. 1, pl. XVI. Consideration of the large size of
this muscle strengthens the conviction that Chlamydoselachus is in the habit of seizing
and swallowing fairly large prey. In this case the superficial constrictor muscles (Text-
figure 70; also Allis, 1923, Fig. 46, pl. XVII, and Fig. 48, pl. XVIII) as well as practically
every other muscle of the oral and branchial region, may be brought into play to assist
in the act of swallowing which is finally completed by the constrictor of the esophagus.
The superficial constrictor muscles that run in the gill flaps are thin (Text-figure 78, p. 421)
but they are broad and they overlap like the shingles on a roof, so that collectively they
may exert considerable pressure. It has already been noted that the labial cartilages
are held in place by strong ligaments and fascia; some of these cartilages serve for the
attachment of special muscles. Thus an integumental muscle, the protractor anguli
oris, has a tendon attached to the mandibular labial cartilage (Allis, 1923). The strong
levator labii superioris (Allis, 1923, pp. 183-184 and Fig. 15, pl. X) may assist the creature
in expanding the mouth opening while swallowing its prey. Of this muscle Allis says:
The levator labii superioris, in all my specimens, is wholly independent of the adductor
mandibulae, my specimens apparently differing in this respect from those examined by
Fiirbringer (1903, p. 384) and Luther. The muscle arises by a relatively long tendon from
the ventro-postero-lateral corner of the ectethmoidal process, and running almost directly
posteriorly swells abruptly into a muscle body which is inserted on the anterior half of the
posterior upper labial, some of the fibers apparently being inserted in the adjacent tissue
of the upper lip. The muscle is innervated, as both Furbringer and Luther have stated,
by a branch of the mandibularis trigemini which arises from that nerve shortly after its
separation from the maxillaris trigemini.
In many selachians there is a fairly strong adductor muscle, related to the mandible,
which is usually referred to as the muscle add. gamma of Vetter’s (1874) description.
In Chlamydoselachus, the long tendinous portion of this muscle is apparently represented
by a strong ligament, which has its origin on a little process of the anterior edge of the
hyomandibular and its insertion on the posterior edge of the postorbital process of the
cranium (Allis, 1923, p. 187 and Fig. 23, pl. XI). I quote the following from Allis, 1923,
pp. 187-188:
Firbringer and Luther both say that this muscle is not found in Chlamydoselachus.
Furbringer accordingly considers it to be a secondary arrangement, possibly the beginning
of a differentiation of a superficial portion of the adductor mandibulae, such as is found in
Amia and in many teleosts. Luther (1909, p. 54) thinks it is developed from the most posterior
portion of the adductor, and he considers it to be an archaic feature (I.c., p. 64) notwith-
standing that he did not find it in either Chlamydoselachus, Echinorhynchus or Odontaspis.
In Squatina, it is to be noted, the muscle arises by a few fibers from the hyomandibula (Luther,
1909, p. 60).
One is especially impressed by the differences, with respect to this muscle add.
gamma, between the closely related forms, Heptanchus and Chlamydoselachus. In
The Anatomy of Chlamydoselachus 399
Heptanchus (Vetter, 1874, Fig. 1, pl. XIV) the muscle is well developed; in Chlamy-
doselachus it is apparently represented by a ligament which is attached, not to the mandi-
ble, but to the hyomandibular. It seems probable that the presence of this muscle, as
in Heptanchus, is primitive for sharks while the related structure in Chlamydoselachus
is a modification that has arisen in connection with the peculiar hyostylism of the jaws.
In attempting to identify homologous muscles in different species of vertebrates,
considerable dependence is placed on their innervation. The motor nerves, growing
outward from the central nervous system, establish connections with the muscles or
pre-muscle masses quite early in their development. Should the muscle subsequently
migrate in order to reach its definitive position, its nerve follows it. Thus in the branchial
region, it is generally considered that all the muscles innervated by the fifth (trigeminal)
nerve are derivatives of the first visceral (the mandibular) arch, while all the muscles
innervated by the seventh (facial) nerve are derivatives of the second visceral (the hyoid)
arch. In most sharks, the musculus intermandibularis is supplied by the mandibular
branch of the trigeminal nerve; but in Chlamydoselachus, Furbringer (1903, Fig. 1, Taf.
XVI) figures the musculus intermandibularis as supplied only by branches of the seventh
(the facial) nerve, and Hawkes (1906) states that “the mandibular ramus [of the trigeminal
nerve] does not supply the large median muscles which lie in the angle made by the two
sides of the lower jaw.” Luther (1909) was unable to trace any branches of the trigeminal
nerve to the intermandibular muscles of Chlamydoselachus, Hexanchus and Heptanchus.
In the notidanids and in Chlamydoselachus, the superficial muscles spanning the halves
of the mandible are supplied by branches of the seventh or facial nerve (Luther, 1909).
For Chlamydoselachus and Heptanchus the distribution of these branches is shown in
Luther’s (1909) Fig. 1, Taf. I, and Text-figs. 9 and 10; for Chlamydoselachus they are
better shown by Allis (1923) in his Fig. 6, pl. WI, which is in color. Luther (1909)
concluded that when the intermandibular muscle is innervated wholly by the nervus
facialis, a muscle of mandibular-arch origin has simply been crowded out by one of hyoid
arch origin; but in his later work (1913, p. 46) Luther decided that the trigeminus muscle
here persisted, but had secondarily acquired innervation by the nervus facialis.
Allis (1917) gave particular attention to this matter of the innervation of the
musculus intermandibularis in Chlamydoselachus and related forms. His conclusions
appear to be embodied in the following statement (Allis, 1917, p. 389):
The interhyoideus and intermandibularis muscles of Chlamydoselachus could accordingly
both be of facialis origin, so far as the relations of nerve and muscle are concerned, but in all
probability only that portion of the intermandibularis that lies anterior to the point where
the nervus facialis definitely disappears from its external surface could be of mandibular
origin. And if this portion of the muscle be of mandibular origin, as several authors have
maintained, I consider it certain that it is innervated by a branch of the nervus mandibularis
trigemini, and that that branch has simply been missed in dissections, my own included.
In the introduction to his 1923 memoir, Allis states: “The investigation of the
nervous system had only just begun, and . . . this part of the cranial anatomy is only
400 Bashford Dean Memorial Volume
5
briefly noticed in the present memoir.” This leaves us in doubt whether Allis made any
further dissections before writing (1923, pp. 188-189):
The muscles innervated by the nervus facialis, all of which are here considered as belong-
ing to the hyal arch, are represented by a single continuous muscle sheet, which is partially
differentiated, by differences in the insertion of its fibers, into a constrictor supertficialis,
a levator hyomandibularis, an interhyoideus and an intermandibularis. . . . These several
portions of the continuous muscle sheet are all apparently innervated exclusively by branches
of the nervus facialis, and there is accordingly no musculus intermandibularis of mandibular
origin in this fish. This has been fully discussed in an earlier work (Allis, 1917), the course
of the ramus hyoideus facialis and its relations to the several muscles there also being given.
Whatever light future investigations may throw on the possible persistence of
a vestigial musculus intermandibularis of mandibular arch origin, the fact remains that
what appears to be the intermandibular muscle of Chlamydoselachus, Hexanchus and
Heptanchus is innervated by a branch of the facial nerve, contrary to what has been
found in all other sharks that have been investigated. This evidence, so far as it goes,
tends to draw Chlamydoselachus and the notidanids closer together and at the same time
to separate them further from other existing sharks.
Considering the small size of the external opening of the spiracle and the absence of
an authentic spiracular cartilage, it is not surprising that we have found no mention of
a special spiracular muscle in Chlamydoselachus. Luther (1909, p. 12) mentions a spirac-
ular muscle in Hexanchus, and in his Fig. 1, Taf. I, it is clearly shown as a prominent
sphincter; but there appears to be no special differentiation of the muscles adjoining the
spiracle of Heptanchus (Luther, 1909, Fig. 2, Taf. I).
An interesting though probably anomalous condition of the musculi interarcuales
dorsales was found by Allis (1915 and 1923) in one of three specimens of Chlamydoselachus
studied by him. In the specimen under consideration, the musculi interarcuales dorsales
form an almost continuous sheet of muscular and ligamentous tissue in the roof of the
pharynx (Text-figure 71). These muscles are better shown in Allis’s (1923) Fig. 56, pl.
XXI, which is drawn from the same specimen but to a larger scale and in color. In the
two other specimens of Chlamydoselachus studied by Allis, the individual muscles of
the interarcuales dorsales group are better differentiated and there is no common sheet
of muscular tissue mesial to the pharyngobranchials. Nevertheless, the related ligamen-
tous sheet existed in the two specimens as in the other one, and “extended the full length
of the branchial region” (Allis, 1915). From one of the two specimens thus described,
Allis’s (1923) Fig. 53, pl. XX, was drawn. The condition shown here is more like what
is found in Heptanchus (Furbringer, 1897, Fig. 1, Taf. V; Davidson, 1918, Fig. 3), where
the muscle is broken up into segments between the respective pharyngobranchial
cartilages. Thus we find, in the musculi interarcuales dorsales of Chlamydoselachus,
one more example of decided variability,
—
The Anatomy of Chlamydoselachus
DIGESTIVE SYSTEM AND ASSOCIATED
ORGANS
There are few published descriptions of the di-
gestive organs of Chlamydoselachus, and these accounts
are very brief. This situation may be due, in part, to
the circumstance that most of the specimens that have
come into the hands of anatomists had been eviscer-
ated. The following account is based mainly on my
studies and drawings of material in the collection of
the American Museum of Natural History, but it in-
cludes a review of the work of other investigators.
My material includes the three large female speci-
mens whose external characteristics have been fully
described by Gudger and Smith (1933). In all these
specimens, the body cavity had been opened by a
ventral longitudinal incision and the digestive tube
had been split open along its length. Thus it was not
possible to view the digestive organs in an undisturbed
condition. In two specimens, the liver was nearly all
missing and the mesenteries had been much torn. The
best-preserved specimen, No. I, had all the digestive
organs, also the spleen, complete; but the mesenteries
were considerably torn. Another large female speci-
men, kindly lent by Dr. E. Grace White, was used
here only for the study of the thyroid, since the di-
gestive organs had been removed. I shall call this
specimen No. IV.
THE DIGESTIVE TUBE
Before proceeding with a description of the vari-
ous parts of the digestive system, it is advisable to
call attention to Text-figure 72, drawn from specimen
No. I, wherein each part of the digestive system, ex-
cepting mouth and pharynx, is drawn to scale in its
approximate relation to the whole. In order to dis-
play certain organs to the best advantage, the natural
position has in some instances been altered. Thus the
lobes of the liver have been drawn aside, the cardiac
stomach has been turned to the left in order to bring
401
Text-figure 72.
The digestive system of Chlamydo-
selachus, ventral aspect, about one-fifth
natural size.
b.e., bursa entiana; c., colon; c.b.d., common bile
duct; c.s., cardiac stomach; d.mes., dorsal
mesentery; d.p., dorsal pancreas; es., esophagus;
g.b., gall bladder; 1.1., left lobe of liver; py.,
pylorus; py.ves., pyloric vestibule; r., rectum;
7.g., rectal gland; 7.1., right lobe of liver; sp.1,
valvular
v.p.,
spleen; sp.2, accessory spleen; v.i.,
intestine; v.mes., ventral mesentery;
ventral pancreas.
Drawn from specimen No. I in the collection of
the American Museum of Natural History.
402 Bashford Dean Memorial Volume
the pyloric vestibule and the pylorus into view, and the rectal gland has been turned to
the left. In this paper, the terms right and left mean the right and left sides of the fish
itself, regardless of its position with respect to the observer.
THE PHARYNX
The mouth, including the teeth, has been adequately described by Gudger and Smith
(1933). The pharynx is of importance for respiration, but since it affords passage for
food it must be briefly considered from this point of view.
The mouth and pharynx of Chlamydoselachus form one large cavity, the oro
pharyngeal cavity. For so slender a shark, the size of this cavity when fully distended
is remarkable (Text-figure 2, p. 337). Although a large mouth does not necessarily
imply that large objects are taken as food, in the case of Chlamydoselachus there is col-
lateral evidence, such as the character of the teeth, indicating that the animal seizes and
swallows living prey of considerable size. It seems likely that the elaborate pharyngeal
musculature, already considered, assists in the act of swallowing the prey, snake-fashion.
Almost the entire oropharyngeal cavity is lined with close-set denticles. On the
lining of the roof, the denticles are exceedingly small. On the floor, especially where
this is upraised to form a structure superficially resembling a rudimentary tongue, the
denticles are appreciably larger. Some of these denticles, in a region overlying the thy-
roid gland, are shown in Text-figures 75 and 76, p. 417. On the inner surfaces of the
gill arches, excepting only the hyoid arch and the dorsal portions of the most posterior
branchial arch, they are particularly large, but are still smaller than those at the angles
of the mouth (Text-figure 10, p. 345), described and figured by Gudger and Smith (1933).
The larger denticles are of the same general character as those of the epidermis; but the
central cusp is longer and sharper, and curves backward. The denticles of the gill-arches
and the floor of the pharynx offer little resistance to a finger tip passed over them in
a cephalocaudad direction, but pierce the epidermis and cling tenaciously when the
finger tip is pulled over them in the opposite direction. Presumably, the pharyngeal
denticles assist the animal in retaining its hold on slippery prey, partly swallowed.
Garman (1885.2) shows denticles on the inner surfaces of the gill-arches of his specimen
(my Text-figure 77, p. 421), but they appear larger than those found in a corresponding
situation in my specimens.
ESOPHAGUS AND CARDIAC STOMACH
As in most elasmobranchs, the wide, distensible esophagus passes without abrupt
demarcation into the large, thin-walled cardiac portion of the stomach. In Chlamydo-
selachus one cannot tell precisely where the esophagus leaves off and the stomach begins.
The combined length of esophagus and cardiac stomach is remarkable (Text-figure 72;
and Table I, p. 412), since together they form about half the total length of the digestive
tube. In my best-preserved specimen, No. I, the collapsed and flattened esophagus is
The Anatomy of Chlamydoselachus 403
about 55 mm. wide where it joins the pharynx, but it narrows rapidly to an almost uniform
width of 30 mm. throughout most of its length. The diameter of the widest portion of
the cardiac stomach is about 45 mm.
In all the specimens in the American Museum,
a previous dissection had shown the stomachs to be
practically empty. Nevertheless in specimen No. II
the cardiac stomach had evidently been hardened
while in a distended condition, since its lumen is un-
usually large and its walls are very thin. In this
specimen, throughout a large portion of what is
presumably cardiac stomach, the wall is only about
1 mm. thick; I suspect, however, that most of the
mucosa is missing. The inner surface is smooth. In
my other specimens the cardiac stomach is less dis-
tended and its wall is appreciably thicker; the inner
surface is cast into slight longitudinal folds. In all
three specimens the thickness of the wall of the car-
diac stomach increases toward its caudal end, but
it is nowhere more than 2 or 3 mm. thick.
On the right side near the caudal end of the
cardiac stomach of Chlamydoselachus, Hawkes (1907)
describes and figures (my Text-figure 73) a more de-
cided thickening (L.T.S.) which she suggests may
be a “lymphatic gland.” Hawkes does not tell how
many specimens she studied, nor whether this thick-
ening occurred in more than one specimen. I have
found no such structure in any of my three speci-
Text-figure 73.
Digestive tube of Chlamydoselachus,
from the middle of the stomach to the
mens. From specimens I and III, I have excised middle of the valvular intestine.
some segments of the slightly thickened wall near B.D., bile duct; B.D.B.E., dotted line showing the
the caudal end of the cardiac stomach, and upon °°" Gf dn Gallas) Gane) Git Cina [Bil Gnesi
H the wall of the bursa entiana; B.E., bursa entiana;
microscopical examination have found only the layers — C.,, caecum at the hinder end of the larger arm
characteristic of a stomach, including an inner eee Fee rane Sees
glandular layer in a poor state of preservation. pyloric valve; S., stomach; S.1. short arm of
Collett (1897) states that in his specimen of ee ae nh
Chlamydoselachus measuring 1910 mm., the stom-
ach proper is small and proportionally narrow; its length is 340 mm., its breadth is
about 45 mm.
In Heptanchus (Daniel, 1934) the stomach is U-shaped or V-shaped, the larger left
limb being the cardiac portion, and the smaller right limb, the pyloric division. In two
of my specimens of Chlamydoselachus a small division, the pyloric vestibule, is inter-
404 Bashford Dean Memorial Volume
posed between the cardiac stomach and the pylorus. It seems probable that, when
present, this division in Chlamydoselachus is homologous with a part of the pyloric
stomach of Heptanchus.
THE PYLORIC VESTIBULE
In my specimen No. I the cardiac stomach narrows considerably near its caudal end.
It is marked off from the next division, which I shall call the pyloric vestibule, by a sharp
constriction. The pyloric vestibule is cylindrical in form and is of smaller caliber than
the cardiac stomach, though decidedly larger than the pylorus. The vestibule leads off
from the dorsal surface of the cardiac stomach, beginning about 10 mm. from its caudal
end, and extends somewhat cephalad, dorsal to the cardiac stomach, for a distance of
about 25 mm., then makes an abrupt turn dorsad and caudad before joining the pylorus
which extends obliquely to the right and caudad. Thus the pyloric vestibule, considered
together with the adjoining portion of the cardiac stomach, is somewhat S-shaped. In
Text-figure 72 the pyloric vestibule (py.ves.) has been exposed by turning the cardiac
stomach to the left. Therefore the vestibule has been rotated through an angle of nearly
90° and appears almost as if viewed, in its natural position, from the right side. In the
specimen under consideration, the pyloric vestibule is about 35 mm. long and (in a col-
lapsed and flattened condition) about 22 mm. wide in its widest portion which is near its
junction with the cardiac stomach. Its wall is about 1.5 mm. thick and is of the same
general character as the wall of the cardiac stomach. The sharp constriction between
the cardiac stomach and the pyloric vestibule is more marked internally since here the
flattened lumen has a width of only 15 mm., which is 4 mm. less than the diameter of the
lumen of the adjoining portion of the pyloric vestibule. At its pyloric end, the vestibule
narrows abruptly to join the pylorus; here, the entrance has the same diameter as the
lumen of the pylorus.
In specimen No. III, the pyloric vestibule is much smaller. It is situated on the
dorsal side of the caudal end of the cardiac stomach. In life it was probably spherical,
but it is now much flattened by pressure between the cardiac stomach and the dorsal
body wall; it has been hardened in that condition. Externally, on its anterior border
it is marked off from the cardiac stomach by a deep groove. Internally, its lumen is
partially separated from that of the cardiac stomach by a crescentic valve-like flap almost
completely encircling the residual lumen but leaving a circular aperture about 15 mm. in
diameter. On the anterior side, where it is best developed, the width of this flap is
about 5mm. I am of the opinion that the flap, as such, is an artifact due to pressure,
since by stretching the wall of the stomach longitudinally the flap may be reduced to
a low fold. There remains, however, a very decided constriction marking off the pyloric
vestibule from the cardiac stomach. An aperture about 4 mm. in diameter leads off from
the anterodorsal side of the pyloric vestibule into the pylorus which extends obliquely
to the right and caudad. The proximal third of the pylorus adheres firmly to the wall
of the pyloric vestibule.
The Anatomy of Chlamydoselachus 405
In specimen No. II there is nothing resembling a pyloric vestibule; the pylorus
comes off abruptly from the caudal end of the cardiac stomach and leads directly backward.
The aperture leading from the cardiac stomach to the pylorus is very small, but admits
a probe without difficulty, The muscular wall surrounding this aperture is unusually
thick; evidently it serves as a sphincter. In the specimen figured by Hawkes (1907)
and reproduced as my Text-figure 73, there is no division of the stomach corresponding
to what I have called the pyloric vestibule. I cannot reconcile this difference further
than to say that here, as in many other structures, Chlamydoselachus shows remarkable
variability.
THE PYLORUS
In all my specimens, the pylorus is a slender portion of the digestive tube which,
from superficial appearances, might more appropriately be designated a part of the small
intestine. However, the region under consideration undoubtedly corresponds to what
is called pylorus in other sharks, as in Galeus (Daniel, 1934, Fig. 135, p. 136). In Chlamy-
doselachus (Text-figure 72) the caudal extremity of the pylorus (py.) projects into the
next division of the digestive tube, the bursa entiana (b.e.), as a large conical papilla, the
pyloric valve. The muscular layers of the pylorus appear to be continuous with similar
layers in the valve. At the summit of the papilla there is an aperture which, in the hard-
ened condition of the material, is still large enough to admit a probe easily. This opening
is the passageway from the pylorus to the bursa entiana. The cone-shaped valve is
asymmetrically placed and adheres, more or less, to one side of the bursa.
On account of the overlapping of the pylorus by the bursa, in recording their lengths
for the purposes of Table I it was necessary to divide the region of overlapping equally
between them. In specimen No. I (Text-figure 72) the overlapping occurs mainly on
one side and is about 6 mm. in its greatest extent; the total length of the pylorus, including
its valve, is 36 mm. The width of the pylorus, in its present collapsed and flattened
condition, is about 8 mm. In specimen No. II the lumen of the bursa entiana overlaps
the pyloric valve for a distance of 14 mm. on one side and 6 mm. on the other. The total
length of the pylorus, including its valve, is 40 mm. In this specimen the pylorus is
cylindrical and its diameter is only 6 mm. In specimen No. III the pylorus is unusually
short. Its valve is overlapped, on one side only, by the lumen of the bursa entiana for
a distance of 6 mm. and its total length is 28 mm. At its widest point, which is near
its middle, the collapsed and flattened pylorus of this specimen measures 12 mm. across.
In specimens I and III the wall of the pylorus is a scant millimeter in thickness; in No. II
it is about 2 mm. thick. In all my specimens the inner surface of the pylorus is traversed
by longitudinal folds. These are more prominent in No. II because of the contracted
condition of the pylorus in this specimen.
Hawkes (1907) describes the division which I have called the pylorus, as follows:
‘The shorter arm of the stomach (S. 1) differs from the larger anatomically and functionally.
It is a short, thick-walled tube incapable of distension, the lining mucosa of which is
406 Bashford Dean Memorial Volume
raised into parallel ridges. This arm opens into the intestine by a protruding pyloric
aperture (Py. V.) which is furnished with distinct sphincter muscles.” The pyloric
valve (Py. V.) figured by Hawkes (my Text-figure 73) appears symmetrical, thin-walled,
slender and cylindrical—quite unlike any that I have observed, save that it protrudes into
the bursa. Possibly the drawing is inaccurate, since the valve appears too thin to be
provided with a sphincter muscle. In Heptanchus (Daniel, 1934, Fig. 123), as in Chlamy-
doselachus, the pyloric valve projects as a well-defined circular band into the bursa.
THE BURSA ENTIANA
In Chlamydoselachus, as in sharks generally, the middle intestine or duodenum is
short; as in certain other elasmobranchs, it is expanded to form a thin-walled sac, the
bursa entiana (Text-figure 72, b. e.). In Chlamydoselachus the bursa entiana is shaped
somewhat. like the human stomach, but the orientation is different. Superficially, it
would resemble the human stomach if the latter were reversed end-for-end and rotated
so that the greater curvature would lie to the right and dorsally. In my three specimens
the amount of distention of the bursa varies greatly, so that the dimensions recorded
here do not give any accurate information as to what the relative size would be if the
structures were measured under identical conditions.
In my specimen No. I the bursa entiana is moderately distended and has moderately
thick walls; its condition is probably typical. Measured from the first coil of the spiral
valve to the apex of the pyloric valve, its length is 33 mm.; but after including the total
extent to which the bursa overlaps the pylorus, the length is 39 mm. Its greatest trans-
verse diameter is about 14 mm. Its walls are very thin (less than 1 mm.) at the cephalic
end, but toward the caudal end the thickness increases gradually to almost 2 mm. at the
junction with the valvular intestine.
In specimen No. II the bursa is greatly contracted. Measured from the villosities
on the inner surface of the cephalic end of the valvular intestine, to the apex of the
pyloric valve, its length is 20mm. Since the bursa overlaps the pyloric valve for a distance
of 14 mm. on one side, its total length is 34 mm. Its greatest transverse diameter is
about 10 mm. The thickness of its walls ranges from 1 mm. at the cephalic end to 3 mm.
at the caudal end.
In specimen No. III the bursa is greatly expanded. Its length, measured from the
cephalic end of the spiral valve to the apex of the pyloric valve, is 40 mm. After in-
cluding the extent to which the bursa overlaps the pyloric valve, the total length is
46mm. The greatest transverse diameter, which is near the caudal end, is about 18 mm.;
near the cephalic end the transverse diameter is about 10 mm. The wall is everywhere
less than 1 mm. thick.
In the lining of the ventral side of the bursa entiana in specimen No. I there is
a pocket (shown by a dotted outline in Text-figure 72) about 10 mm. long, opening caudad
into the lumen of the bursa. The opening is about 8 mm. wide and is situated about
The Anatomy of Chlamydoselachus 407
one-third of the distance from the apex of the pyloric valve to the beginning of the valvu-
lar intestine. A probe inserted into the pocket readily entered the common bile duct
(c.b.d.) which extends anteriorly. A similar but slightly larger pocket occurs in specimen
No. III; it is situated a little further caudad, rather more than halfway toward the valvular
intestine. A probe passed into this pocket did not find the opening of the bile duct.
A bile duct could not be found in the vicinity, but this was probably because the region
had been mutilated. In specimen No. II the pocket, as such, could not be found, but
a channel or canal leads from the cephalic end of the valvular intestine into the rather
thick, contracted wall of the bursa entiana. This channel was probed. After proceeding
for a distance of about 15 mm. cephalad within the wall of the bursa, the probe entered
the bile duct which extends anteriorly. The channel is, therefore, an extension of the
bile duct caudad within the wall of the bursa entiana.
In specimen No. I the inner surface of the bursa is fairly smooth save in a region
extending caudad from the pocket which forms the opening of the bile duct. This area
is traversed by longitudinal folds similar to those shown in Text-figure 73. In specimen
No. I, these folds extend along the inner surface of the outer wall of the pocket and are
visible through its thin inner wall. In specimen No. III, where the bursa is greatly
expanded, its inner surface is smooth except that the area which in specimen No. I is
cast into longitudinal folds, is here somewhat rough and flaccid. In specimen No. II,
where the bursa is strongly contracted, its entire inner surface is cast into strong lon-
gitudinal folds. The longitudinal canal within the wall of the bursa, which communi-
cates with the bile duct anteriorly and opens into the valvular intestine posteriorly, was
opened by a longitudinal incision after it had been probed. Its inner surface is very
rough, with many small papillae like those found in the upper end of the valvular in-
testine. Thus, in the character of its lining, this channel resembles the valvular intestine
and differs from the bursa entiana. It constitutes a decided variation from the usual
condition in which the bile duct enters the bursa entiana through a funnel-shaped pocket.
Hawkes (1907) described and figured (my Text-figure 73) a pocket situated nearer
the valvular intestine than the pockets described in my specimens No. Iand III. The
flap forming the inner wall of the pocket figured by Hawkes is not so well developed as
in my specimens I and III, where its free edge extends in a straight line transversely
or somewhat obliquely. The condition that I have described in specimen No. IJ, whereby
the bile is conveyed through a special channel in the wall of the bursa directly into the
valvular intestine, apparently has not been observed by any other investigator.
In Heptanchus (Daniel, 1934, Figs. 120 and 123) the middle intestine or duodenum,
corresponding to the bursa entiana of Chlamydoselachus, is not sharply marked off from
the valvular intestine. Daniel (p. 124) states that “the valve of the spiral intestine extends
forward throughout the length of the middle intestine and touches the pyloric valve.”
This contrasts strongly with the simpler condition in Chlamydoselachus, already
described.
408 Bashford Dean Memorial Volume
THE VALVULAR INTESTINE
In my three specimens the valvular portion of the digestive tube is spindle-shaped,
but tapers much more rapidly in its caudal half; the cephalic end is almost truncate.
Gunther's (1887) figure (my Figure 15, plate IV) gives proportions similar to those found
in my specimens save that in his dissection the valvular intestine is laid widely open
after being slit longitudinally. In my specimens the external surface of the valvular
intestine is either bluish-gray or brown, appearing much darker than the other portions
of the digestive tube. The walls are very thick, ranging from 5 or 6 mm. near the cephalic
end, to 1 or 2 mm. at the caudal end where it joins the colon. In two of these speci-
mens the spiral valve extends to the extreme cephalic end of the thick-walled portion
of the digestive tube, but in No. II the spiral valve stops at about 20 mm. from the ceph-
alic end of the thick-walled portion. For the remaining distance the inner surface
shows villosities similar to, but larger than, those found in the region of the spiral valve.
On this account, and also because of the thickness of its walls, this part is assigned to the
valvular intestine. For similar reasons I have included with the valvular intestine a short
thick-walled portion, with a velvety lining, between the caudal end of the spiral valve
and the thin-walled colon. In specimens I and III the length of this region is 15 mm.;
in No. Ilitis 20mm. The posterior four-fifths of the valvular intestine lacks a mesentery.
In my specimen No. I, the form of the valvular intestine seems perfectly preserved.
The maximum diameter is only 26 mm., while the length is 190 mm. In No. II the val-
vular intestine is much larger; its maximum diameter is about 33 mm., while its length
is 240 mm. In No. III the organ is about the same size as in No. II, but is so irregularly
molded that its diameter cannot be accurately measured.
In Chlamydoselachus the spiral valve is a continuous ribbon-like structure attached
by one edge to the inside of the wall of the intestine, while the other edge is either free,
winding about a central cavity, or is attached to an axial strand. In specimen No. |
the anterior third of the spiral valve has a central cavity large enough to admit a pencil;
the posterior third has a much smaller central cavity, while the middle third has an axial
strand. In specimen No. IJ a central cavity alternates with an axial strand at irregular
intervals. In specimen No. III there is a central cavity of moderate size extending the
entire length of the spiral valve except in its middle portion, where there is a short axial
strand. In the specimen portrayed by Gunther (my Figure 15, plate IV) it is clear that
there is a central cavity in the caudal half and at the cephalic end, while the interval
between has possibly an axial strand.
In its natural position, the spiral valve of Chlamydoselachus does not lie vertical
to the wall of the intestine: it slants either forward or backward. Thus each coil has the
form of an asymmetrical cone, of which the apex may be missing. When the intestine
is contracted, the spiral valve makes an acute angle with the wall of the intestine; when
it is expanded, the spiral valve may be drawn into a nearly transverse position.
The Anatomy of Chlamydoselachus 409
In my best-preserved specimen, No. I, there are 44 coils of the spiral valve. In the
nine anterior coils, the angle is very acute and the cones point cephalad; in the remaining
coils the cones point acutely caudad. The transition between the two conditions is
abrupt. In specimen No. II there are 45 coils; each of these makes an acute angle with
the wall of the intestine, and points caudad. In specimen No. III there are 37 coils. In
the anterior third, the coils or cones are obtuse but point definitely cephalad; those of
the posterior third are acute and point caudad; while those in the middle third are
apparently transverse, but this region is much distended and is poorly preserved. In
this specimen the transitions between the regions described are gradual.
Gunther’s (1887) Fig. 5, pl. LXV (my Figure 15, plate IV) shows 35 coils in the
spiral valve of Chlamydoselachus. Of these, the first 19 point forward, one is transverse,
and the remaining 15 point backward. Collett (1897, p. 13) states that in his specimen
“the intestine (colon) is cylindrical, very muscular, and contains 47 spiral valves.” In
a specimen described by Hawkes (1907) there are 43 coils: the first 7 (my Text-figure 73)
point forward, one is contorted, and the remaining 35 are directed backward. Hawkes
points out that the inclination of the spiral valve has a physiological significance: where
the valve is directed forward the passage of the food is undoubtedly slower than where
it is directed backward.
In Heptanchus maculatus (Daniel, 1934, Fig. 123 and pp. 124-125) the spiral valve
makes 17 or 18 turns. The folds are far apart anteriorly and very much closer posteriorly.
The valve is considerably broader than the diameter of the intestine and is thrown into
a series of cones having their apices pointed anteriorly. The surface of the valve, viewed
under the microscope, shows numerous finger-like villi.
It has been noted in Chlamydoselachus that the anterior coils of the spiral valve
usually point forward, and the posterior coils usually point backward. This condition
of the spiral valve seems to be exceptional among elasmobranchs. A similar condition
has been found (Parker, 1885) in a single specimen of Scylliwm canicula, and something
like it occurs in Zygaena (Parker, 1885, Fig. 8, pl. XI). In most sharks the apices of prac-
tically all the coils point forward, as in Scyllium (Parker, 1885, Fig. 5, pl. XI); or backward,
as in Heptranchias perlo (Garman, 1913, Fig. 1, pl. 58). In some specimens of Raja (Parker,
1885) the apices of all the coils point forward, while in other specimens all but the first
coil are deflected backward. Moreover in some sharks, as in Cephaloscyllivm umbratile
(Garman, 1913, Fig. 2, pl. 58), and in some specimens of Raja (Parker, 1885), an axial
cord extends the entire length of the valvular intestine. In other sharks, as in Isurus
punctatus (Garman, 1913, Fig. 3, pl. 58), and in other specimens of Raja (Parker, 1885),
there is instead an axial tube. Both axial cord and axial tube occur, in Chlamydoselachus,
in each individual specimen, where they are restricted to different parts of the valvular
intestine. Thus in the valvular intestine of Chlamydoselachus there are combinations of
features that almost always occur separately in other elasmobranchs. This affords
a striking example of the structural comprehensiveness usually considered characteristic
of the more archaic members of a phylum or class.
410 Bashford Dean Memorial Volume
RECTUM AND RECTAL GLAND
In most elasmobranchs the portion of the digestive tube extending from the valvular
intestine to the anal opening is differentiated into two parts, colon and rectum. In
conformity with the usual practice I have distinguished two regions, colon (c.) and
rectum (r.), in Text-figure 72; but these parts are much alike and there is no definite
boundary between them, therefore I shall here consider the two regions, combined, under
the term rectum.
The lengths, in my three specimens, are given in Table I, p. 412. It will be noticed
that in specimen No. II the rectum is unusually long. In each specimen, the width of the
rectum is about the same throughout its length, so that in ventral view it appears to be of
uniform diameter; but when viewed from the side, the rectum appears somewhat funnel-
shaped since it enlarges toward the anus. In specimen No. | the rectum is 9 mm. wide
and has a dorsoventral diameter of 13 mm. at its cephalic end, 16 mm. at its middle, and
20 mm. at the anal end. Similar proportions are found in my other specimens. In speci
men No. II the rectum is 6 mm. wide; its dorsoventral diameter is 10 mm. at the cephalic
end, and 16 mm. at the anal end. In specimen No. III the width is 8 mm.; the dorso-
ventral diameter is 10 mm. at the cephalic end, and 18 mm. at the anal end. From these
dimensions it is evident that in each case the rectum is laterally compressed, and dorso-
ventrally enlarged toward the anus. The anal opening faces both ventrad and caudad,
so that it leads directly to the exterior and also into the cloaca. The wall of the rectum
is from 1 to 2 mm. thick. The lining is cast into slight longitudinal folds which are more
pronounced in specimen No. I. There is no mesorectum save the very small mesentery
supporting the rectal gland, at the extreme caudal end of the rectum.
The rectal gland is a laterally compressed, somewhat kidney-shaped body situated
in the angle between the rectum and the cloaca. In Text-figure 72 the rectal gland
(r.g.) is shown turned toward the left. The dimensions in my three specimens are: No.
I, 20x 13 x 6 mm:; No. II, 18 x 14x 7 mm:; No. IJ], 17 x 12 x9 mm. The duct leads
anteriorly and ventrally to open into the dorsal side of the rectum. In all three specimens
the duct is 13 mm. long. The opening is distinctly visible on the inner surface of the
rectum; it is guarded by a valve-like flap and readily admits a probe which passes easily
into the rectal gland. In specimen No. I the opening is situated 20 mm. from the valvular
intestine, just midway in the length of the rectum. In specimen No. II the opening is
situated 40 mm. from the valvular intestine, also at the middle of the rectum. In speci-
men No. III the opening is situated 15 mm. from the valvular intestine and 25 mm.
from the anus.
The proximity of the rectal gland to the cloaca has led to its being figured with the
reproductive system. Thus Garman (1885.2) shows in his Fig. 2, pl. XIX (reproduced
as my Text-figure 92, p. 440) an organ labeled “caecal pouch” which corresponds with
what I have called the rectal gland. He does not describe its duct, but in his Fig. 3, pl.
XIX a duct appears to open from this gland into the rectum. Gunther (1887) figures
a gland (my Figure 19, plate V) in the position of a rectal gland, and asserts that it opens
The Anatomy of Chlamydoselachus 411
into the cloaca. Hawkes (1907) states that, in two specimens studied by her, the rectal
gland opens into the rectum. It is so shown in her diagrammatic figure of the female
cloacal region reproduced as Text-figure 90a, p. 435). The function of the rectal gland
is unknown.
In Heptanchus (Daniel, 1934) the portion of the digestive tube between the valvular
intestine and the anus is divided into two parts, colon and rectum. The two parts are
much alike, but the form of the colon is slightly bulbous. The duct of the rectal gland
reaches the wall of the rectum at its cephalic end, but does not enter here; it courses
cephalad in the wall of the colon to enter the lumen at the caudal end of the valvular
intestine.
THE DIGESTIVE TUBE AS A WHOLE
We have seen that the digestive tube of Chlamydoselachus is but slightly longer
than the body cavity, and that all its parts, save only the valvular intestine, are more or
less flaccid when empty. This leaves some doubt as to the precise form of the tube in
its natural position, both when empty and when distended with food. In all my speci-
mens the digestive tube isempty. In specimen No. I, which has a well-developed pyloric
vestibule, there is an abrupt S-shaped fold of the pyloric vestibule and related portion
of the cardiac stomach, in what appears to be the natural position of these organs. In
specimen No. IJ, which has a shorter pyloric vestibule, the smaller fold in the same region
cannot be straightened out. There are no other folds that appear to be of a permanent
nature, but in all my specimens there is considerable irregular folding in the walls of the
cardiac stomach. The question arises whether the distention of this organ with food
would be sufficient to take up whatever “‘slack”’ exists in this region.
Table I gives the total length of the digestive tube, also the length of the body
cavity excluding the small portions along the sides of the cloaca, in my three specimens.
In specimen No. I the digestive tube is 100 mm. longer than the body cavity; in No. I
it is 105 mm. longer; in No. I] it is 203 mm. longer. In No. Iand in No. HI the recurrent
course of the pyloric vestibule takes care of a small part of the excess length. It is probable
that, in specimens I and II, when the cardiac stomach was fully distended with food the
digestive tube became approximately straight; but the same statement could hardly
apply to specimen No. III.
Gunther (1887) writes of Chlamydoselachus: ‘‘The stomach is an extremely long
cylindrical sack with thin walls; the short and narrow intestine, after having made a short
and incomplete convolution, passes into the dilated portion which contains the spiral
valve.”’ I have found no evidence of folding of the intestine in any of my specimens, and
it seems possible that the “short and incomplete convolution” mentioned by Gunther
really belonged to a pyloric vestibule. Collett (1897) states that the intestinal canal of
his specimen is almost straight throughout its length, only the short duodenum being
turned aside between the pylorus and the dilated portion with the spiral valve. Deinega’s
half-tone reproduction (1925, Fig. 1) of a drawing of the viscera in situ is printed on
412 Bashford Dean Memorial Volume
unsuitable paper and details are obscure. The digestive tube appears as a nearly straight
tube in which three main regions are recognizable; there is possibly a small convolution
in the region of transition from stomach to intestine.
A continuous median dorsal mesentery, more fully described in the section on the
urogenital system, supports the digestive tube of Chlamydoselachus throughout its
its length excepting the posterior four-fifths of the valvular intestine and the entire
rectum. The rectal gland has a special mesentery which is evidently an isolated division
of the dorsal mesentery. The mesentery supporting the common bile duct appears to be
a ventral mesentery, but in my specimens it is considerably mutilated and some of its re-
lations are obscure.
TABLE I
Length (in millimeters) of the digestive tube and its divisions in comparison with the total body length
and the length of the body cavity anterior to the cloacal aperture, in three adult female specimens of
Chlamydoselachus.
|
Specimen | Total Body Esophagus | Pyloric Bursa Valvular | Colon and Total
Sern Body
| Number | Length | and Cardia| Vestibule | PY!IOS | Entiona | Intestine | Rectum meee Cay
| u
I 1350 330 35 33 6 190 40 664 =O) C564
Ul 1485 365 Absent 33 2 240 80 745 640
Il 1550 440 | 25 25 3 230 40 803 | 600
THE LIVER
In my specimens II and III the liver is nearly all missing; but in No. I the liver is
intact and (macroscopically) in an excellent state of preservation. Therefore my descrip-
tion is based entirely on a study of specimen No. I.
The liver of Chlamydoselachus (Text-figure 72) is a very large organ. It consists
mainly of two lobes (r.l. and I.1.), one on each side of the body, extending the entire
length (about 600 mm.) of the body cavity including the portions lateral to the cloaca.
At their anterior ends, these lobes are continuous with the short unpaired portion of the
liver which is median in position. The lobes are of equal size and alike in form save that
there is a slight excavation near the distal end of the left lobe. Thus the form of the
liver is decidedly symmetrical. Each lobe is flattened; the greatest width of a lobe is
about 50 mm., but the thickness does not exceed 12 mm. In Text-figure 72 the lobes are
shown in broad view, but in their naturai position they would probably appear in an
edge view. The unpaired portion of the liver is about 60 mm. wide, 55 mm. long, and
8 mm. thick; it is wrapped about the ventral and lateral surfaces of the esophagus. The
gall bladder (g.b.) is 42 mm. long and 16 mm. wide. It is attached to the ventral and
median surface of the unpaired portion of the liver, and projects slightly beyond its
caudal margin.
The Anatomy of Chlamydoselachus 413
A large duct, the common bile duct (c.b.d.), leaves the right lobe of the liver about
260 mm. from its anterior end to course within the ventral mesentery. Its course is
shown in Text-figure 72; it empties into the pocket of the bursa entiana (b.e.). From the
point where it leaves the right lobe of the liver, the duct was traced by palpation and
dissection cephalad to the gall bladder. Its opening was found on the inside of the gall
bladder, and a probe was passed through this opening into the duct. There is no duct
visible at the surface, or leaving the surface, of the left lobe of the liver.
Gunther (1887) states that the liver of Chlamydoselachus consists of two extremely
long lobes which reach backward to the end of the abdominal cavity, and anteriorly
receive the gall bladder between them. Hawkes (1907) writes that the liver consists of
right, left and median lobes. The gall bladder is situated in the median lobe. The
length of the lobes necessitates their being doubled upon themselves. Evidently these
statements are based on more than one specimen, for she writes that in one specimen
the end of the left lobe was found lying on the right side of the body.
Of his 1910-mm. specimen of Chlamydoselachus, one of the largest ever salem
Collett (1897) writes that the liver was enormous. Two and one-half months after the
death of the fish, when it had presumably lost considerable oil, this liver weighed 4250
grams. It consisted of two parallel and symmetrical lobes, the symphysis being 140 mm.
long. Its total length was 950 mm.—nearly one-half the total length of the fish. The
lobes were of equal thickness, and without side lobes except toward the end, where
there was a small side flap. The height of each lobe was 100 mm., and the thickness
55 mm.; their upper (dorsal) edges were somewhat flattened, almost lamellar, while
their lower (ventral) edges were smooth and rounded.
Deinega (1925, Fig. 1) shows, rather indistinctly, a liver of Chlamydoselachus similar
to the one I have described, save that the gall bladder is larger. In Heptanchus (Daniel,
1934, Fig. 119) the liver is constructed on the same general plan, but the lobes are shorter
and relatively thicker than in Chlamydoselachus.
THE PANCREAS
In Chlamydoselachus, as in other sharks and in the embryos of higher vertebrates,
there are two pancreases, dorsal and ventral respectively (Text-figure 72, d.p. and v.p.).
The ventral pancreas is closely related to what appears to be a ventral mesentery, while
the dorsal pancreas is supported by a special mesentery which seems to be a part of the
dorsal mesentery. But in each of my specimens these mesenteries are considerably muti
lated and the digestive tube is free to rotate. The dorsal pancreas is present in all my
three specimens. The ventral pancreas is present in only two; in the other specimen,
the absence of the ventral pancreas is evidently the result of mutilation. In my two
specimens possessing a ventral pancreas, it is combined with an accessory spleen.
The dorsal pancreas is a flattened organ, irregular but somewhat triangular in shape,
situated near the anterior part of the valvular intestine which it slightly overlaps, and
414 Bashford Dean Memorial Volume
very close to the bursa entiana. In its natural position the dorsal pancreas tends to curl
around these organs, but in Text-figure 72 it (d.p.) is shown displaced to the left and spread
out flat. In my best-preserved specimen (No. 1) the dorsal pancreas measures 45 x 25
x 2mm. In my other specimens it is of approximately the same size, but is mutilated so
that precise measurements are impossible. A piece of the dorsal pancreas from specimen
No. I was removed for sectioning. Under the microscope the sections show, on one side,
alveoli characteristic of a pancreas, but I was unable to identify the ducts. Considering
that the material had been preserved for thirty years, the structure of the alveoli is
surprisingly well preserved. On the other side of each section I found areolar tissue,
blood vessels, cords of epithelioid cells and scattered epithelioid cells. This portion may
possibly represent an organ of internal secretion.
In my specimens, the ventral pancreas is easily distinguished from the accessory
spleen, to which it is closely attached, by a difference in color: the ventral pancreas,
like the dorsal pancreas, is pale yellow, while the accessory spleen, like the spleen proper,
is very dark. Together, the ventral pancreas and the accessory spleen form a slender,
somewhat crescentic, slightly-flattened body whose approximate position is shown in
Text-figure 72 (v.p. and sp. 2). In specimen No. | this duplex organ is 40 mm. long
by 8 mm. wide at its widest level; in specimen No. IJ it is 70 mm. long by 10 mm.wide.
The ventral pancreas and the accessory spleen are of equal length and width, and are
united side-by-side; thus they appear as a single organ divided into two longitudinal
zones. From specimen No. I, segments were cut from the light zone and the dark zone
separately, and sections were prepared for microscopical examination. The light zone
was found to be in a very poor state of preservation, but is undoubtedly glandular. It
contains cords of epithelial cells, groups of cells which may represent alveoli, and cells
arranged so as to give the appearance of ducts; also scattered epithelioid cells and many
small blood vessels. A fairly large artery runs along one side of each section. The
dark zone is in a much better state of preservation. It consists mainly of dense lymphoid
tissue containing a multitude of leucocytes and many extravascular erythrocytes. These
observations seem sufficient to identify the organ as a spleen.
From specimen No. I a segment extending entirely across the duplex organ (ventral
pancreas and accessory spleen) was cut into transverse serial sections. The material
is in poor condition for histological study, but one side of each section is undoubtedly
pancreas, the other, spleen. Each organ has a connective tissue capsule. In places the
two organs are connected by their capsules, in other places the capsules are separated
by a cleft.
So far as I know, this combination of a ventral pancreas with an accessory spleen
has not been observed in any other elasmobranch. In the teleost, Gambusia patruelis,
the mingling of spleen and pancreas is described by Potter and Medlen (1935) from whose
paper I quote as follows: “The typical histological structure of this organ [the spleen]
is modified by the presence of pancreatic tissue. The pancreas is located in the mesen-
The Anatomy of Chlamydoselachus 415
teries of the organs in this region, and it penetrates the substance of the spleen by fol-
lowing the blood vessels which supply this organ.”
I was unable to find, by dissection, any undoubted pancreatic ducts. Such ducts
are presumably present, unless they have disintegrated through long preservation of the
material. Hawkes (1907) does not mention any pancreas in Chlamydoselachus, but
describes a pancreatic duct which probably belongs to the dorsal pancreas since it opens
into the valvular intestine where the spiral valve begins.
Collett’s (1897) description of the pancreas in his specimen of Chlamydoselachus is
interesting in that he speaks of dark and light portions of the pancreas. His description
is quoted in full:
The pancreas consists of two large lobes, of which each is subdivided into an upper
and lower portion, so that it really is in four divisions, of which the two hinder portions are
lighter in color than the front ones. On the right side it forms, first, a short light-colored
lobe, about 80 mm. long and 35 mm. broad. Anteriorly, it is almost entirely separated from
a curved front portion, which is of darker hue than the hinder part. Posteriorly there also
exists a lower portion, of a length of about 100 mm.; above this lies a darker-colored portion
whose length is about 48 mm., which adjoins the hinder lighter part, and is connected with it.
Although Collett does not mention a spleen, it seems likely that the dark organs
described by him are accessory spleens.
Deinega’s (1925) drawing (his Fig. 1) of the digestive system of Chlamydoselachus
does not show any organ labeled pancreas, but his Fig. 2 is a drawing of a section of some
tissue said to have been taken near the pancreas. In it he distinguishes blood vessels,
fibers and cells. He suggests that it may be splenic tissue. Evidently this material was
in a very poor state of preservation for microscopical study.
In Heptanchus (Daniel, 1934, Fig. 119) both dorsal and ventral pancreases are present
and well developed. Their relations, as shown in this figure, appear to be much the same
as in Chlamydoselachus. In another figure by Daniel (1934, Fig. 120) the names of the
two divisions of the pancreas appear to have been interchanged.
ORGANS ASSOCIATED WITH THE DIGESTIVE TRACT
For convenience there are included in this section brief descriptions of two organs
that are topographically related to the digestive system, but are not a part of it: the
thyroid gland, which develops from the distal portion of a diverticulum from the floor
of the pharynx; and the spleen, which has no developmental relation to any part of
he digestive system.
THE THYROID GLAND
The position of the thyroid, attached to the ventral surface of the basihyoid cartilage,
is shown in my Text-figure 26a, p. 361, after Goodey, 1910.1; also by Goodey (1910.2)
in his Fig. 1; and by Allis (1923) in his Fig. 38, pl. XIV.
The thyroid of Chlamydoselachus is especially interesting because, in the adult,
it sometimes retains a primitive or embryonic feature. Phylogenetically, the thyroid is
416 Bashford Dean Memorial Volume
regarded as a derivative of a median trough-like fold, the endostyle, such as is found in the
floor of the pharynx in Amphioxus and the ascidians. In all vertebrates in which the
ontogenetic development of the thyroid has been studied, it arises in the embryo (thr.,
Text-figure 62, p. 388) as an outpocketing from the floor of the pharynx. The distal
portion of the outpocketing becomes the thyroid gland. The slender stalk persists for
a time either as a hollow tube, the so-called thyroglossal duct, or as a solid cord; but
eventually it degenerates and disappears. Goodey (1910.2) made the remarkable dis-
covery, in an adult Chlamydoselachus, of a persistent thyroid duct (my Text-figure 74,
v.t.) opening into the pharynx through a perforation in the basihyoid cartilage, and ending
blindly where it comes into contact with the thyroid. This, of course, is not a functional
duct; but it is comparable to the “‘thyroglossal duct” found in the embryos of many
vertebrates. The so-called duct is lined with pharyngeal mucous membrane in which
are numerous incompletely developed pharyngeal denticles.
Text-figure 74.
Sagittal section (x 15) through the thyroid
gland and persistent thyroglossal duct of
an adult Chlamydoselachus.
b.v., blood vessels; d., denticles; e., enamel organ; fo.,
follicles; |.t., lumen of tube; v.t., vestigial tube (thyro-
glossal duct).
After Goodey, 1910.2, Fig. 2.
Since Goodey’s account of the thyroglossal duct of Chlamydoselachus appears to be
based on a single specimen, I have thought it worth while to investigate the possible
occurrence of such a duct in the four large specimens at my disposal. From each specimen
the thyroid was excised together with a large block of surrounding tissues including
a portion of the basihyoid cartilage and the lining of the pharynx. The material was
partially decalcified, then imbedded in celloidin and cut into serial sagittal sections.
In each case the series extended completely through the large foramen in the basihyoid
overlying the thyroid. In one case only (specimen No. I) there were two foramina; the
anterior foramen is very small. This specimen, No. I, is the only one in which a thyro-
glossal duct was found (Text-figure 75, d.), and this duct lies within the posterior and
larger foramen. In specimens III and IV, a thyroglossal duct is demonstrably absent.
In specimen No. II the material is in such poor condition that neither the presence nor
the absence of a duct could be determined.
In the series of sections from specimen No. I, the lumen of the thyroglossal duct is
slightly tortuous, so that the continuity of the duct cannot be demonstrated in any
single section. Text-figure 75, representing the thyroglossal duct, is a reconstruction
from forty successive sections, each about 20 microns thick, and is slightly diagrammatic.
The total thickness of the sections used in this reconstruction is about 800 microns
417
The Anatomy of Chlamydyselachus
WMZZA!
2
Text
Median sagittal section (x 12)
figure 75.
showing thyroid gland and thyroglossal
duct of an adult Chlamydoselachus.
thyroglossal duct; p.d., pharyngeal denticle; thyr.,
thyroid gland.
Drawn from Specimen No. I in the collection of the American Museum of Natural History.
c., basihyoid cartilage; d.,
a., artery;
h
showing thyroid gland of an adult Chlamydoselachus in whic
Median sagittal section (x 10)
there was no thyroglossal duct.
; p. d., pharyngeal denticle; thyr., thyroid; v., vein.
Drawn from Specimen No, III in the collection of the American Museum of Natural History.
a., artery; c., basihyoid cartilage
418 Bashford Dean Memorial Volume
(less than a millimeter). The finer structure of this specimen is rather poorly preserved,
but permits of the following observations. The duct (d.) is lined with stratified squamous
epithelium continuous with the epithelial lining of the pharynx. The outer layer of the
duct consists of a thick layer of dense connective tissue continuous with a similar layer
comprising the deeper portion of the mucous membrane of the pharynx. Between the
epithelium of the duct and its connective tissue layer, there are many calcifications having
the form of rudimentary denticles. These are smaller than the fully developed denticles
(p.d.) that occur in the lining of the pharynx. The distal end of the duct ends blindly
in close contact with the thyroid (thyr.).
Text-figure 76 is a drawing of the thyroid of one of my specimens (No. III) in which
a thyroglossal duct is absent. The histological condition of this material, also, is rather
poor, but the topographical relations are well shown. Upon comparing Text-figures 76
and 75, it will be seen that in specimens I and III the position of the main mass of
the thyroid (thyr.) with respect to the large foramen in the basihyoid cartilage (c.) is not
quite the same.
In specimen No. IV a large part of the thyroid was cut away in trimming the block
preparatory to imbedding, but in the remaining portion the finer structure is well preserv-
ed. While the simple cuboidal epithelium of the follicles is in good condition, the lumens
of the follicles appear empty, as they do in the other specimens. In the sections of No.
IV, the pharyngeal denticles are beautifully shown. In all the sections, the epithelial
lining of the pharynx is very poorly preserved. Fundamentally, it is stratified epithelium,
but it contains many unusually large pale cells, singly or in groups, which are probably
mucous cells.
In Heptanchus (Daniel, 1934, p. 123) the thyroid gland is located “at the symphysis
of the lower jaws between the coracomandibularis and coracohyoideus muscles.” Fergu-
son (1911), after studying many species of elasmobranchs, states that “The [thyroid]
gland rests upon the basihyal cartilage whose anterior margin forms an excellent guide
to its location.” His paper deals with the histological structure as well as the form and
gross anatomical relations of the thyroid in elasmobranchs, and includes a description of
the blood vessels supplying the thyroid. In Scyllium catulus and in S. canicula (Goodey,
1910.2), the thyroid gland is situated close to a foramen in the basihyoid cartilage. In
both species of Scyllium the connective tissue investment of the thyroid extends into
the foramen as a plug containing, in some instances, a small amount of thyroid tissue,
and in one instance, a problematical duct. So far as our present knowledge extends,
Chlamydoselachus is the only vertebrate possessing, at least occasionally, a persistent
thyroglossal duct.
THE SPLEEN
In Chlamydoselachus the spleen proper (Text-figure 72, sp.1) is a very elongate,
somewhat comma-shaped, flattened organ lying in the dorsal mesentery at the level of
the pylorus, pyloric vestibule, and caudal end of the cardiac stomach. In its natural
The Anatomy of Chlamydoselachus 419
position it is probably somewhat coiled about these portions of the digestive tube, but
in Text-figure 72 it is shown displaced to the left. The color of the spleen, in my pre-
served specimens, is a very dark bluish-gray. In my specimen No. I the spleen measures
80 x 10 x 3 mm.; in No. II, 60 x 10 x 4 mm.; in No. III the spleen could not be found and
had evidently been torn away.
From specimen No. I, a transverse segment of the spleen was removed for sectioning.
Under the microscope the sections were found to consist mainly of lymphoid tissue con-
taining an abundance of leucocytes and many extravascular erythrocytes; small arteries
and veins were distinguishable. In its finer structure the spleen proper is very much
like the accessory spleen already described in association with the ventral pancreas.
Hawkes (1907) states that the spleen of Chlamydoselachus is divided into two parts
which are separated by a space of 40 mm. The additional “lobe” (which is apparently
comparable to what I have called the accessory spleen) is situated to the right of the
stomach and somewhat dorsally. It is an ovoid body, 30 mm. long and nearly 20 mm.
broad in its widest part, and is situated between the stomach and a fold of mesentery
which supports the latter. The other part or spleen proper lies in the usual place at the
angle of the stomach. The spleen proper, when examined by a low-power lens, presents
the usual appearance; but the additional “lobe” is much more compact. Hawkes does
not mention a pancreas in association with the secondary spleen.
In Chlamydoselachus, Deinega (1925, Fig. 1) shows, indistinctly, an organ labeled
spleen, which appears to be on the right side of the body since it is crossed by the common
bile duct on its way from the right lobe of the liver to the intestine. In Heptanchus, the
spleen (Daniel, 1934, Figs. 119 and 120) is much more extensive, and is broken up into
several different parts or “lobes.”
In concluding this section I note that the digestive system of Chlamydoselachus
presents the following features of especial interest: (1) The great variability in the
region of transition from stomach to intestine; (2) the differentiation of the coils of the
spiral valve into two series, with apices facing in different directions; (3) the presence
of an axial strand in the middle portion of the valvular intestine, along with an axial
tube in both anterior and posterior portions; (4) the great length of the lobes of the
liver, in adaptation to the form of the body; (5) variations in the position of the opening
of the common bile duct into the intestine; and (6) the presence of an accessory spleen
associated with the ventral pancreas. In some specimens, there is (7) a persistent thyro-
glossal duct which is lined with stratified squamous epithelium and which possesses
rudimentary denticles.
THE RESPIRATORY ORGANS
In Chlamydoselachus, as in other fishes, the gill- filaments and their lamellae are the
primary organs of respiration. Accessory structures such as the branchial skeleton and
musculature, the oral breathing valve and the valvular gill-folds or gill-flaps, are concerned
420 Bashford Dean Memorial Volume
with regulating the passage of water, subservient to respiration, through the mouth into
the pharynx and out through the gill-clefts. When the spiracular canal and external
spiracular orifices of Chlamydoselachus are sufficiently large, doubtless a little water is
expelled through the spiracles. The oral breathing valve, the external openings of the
spiracles, and the gillflaps have been described by Gudger and Smith (1933). In the
present paper I have already described the skeleton and muscles of the oral and pharyn-
geal region, and have noted the absence of a true spiracular cartilage. It remains to
describe the gill-filaments in relation to their supporting structures—in other words,
the gills—and to complete the description of the spiracles. The blood vessels of the
gills are described in the section on the blood-vascular system. My own observations
and drawings of the respiratory system of Chlamydoselachus are based on the three large
specimens in the collection of the American Museum of Natural History, and a fourth
large specimen kindly lent by Dr. E. Grace White.
THE GILLS
From the descriptions and illustrations in the article by Gudger and Smith (1933)
it is apparent that the gill-clefts of Chlamydoselachus are unusually large in proportion
to the size of the body. Some idea of the size of these clefts may be obtained from Text-
figures 4 (p. 339) and 77. Of his specimen Garman (1885.2) writes: “The gill-openings
are large; the first, when extended, will admit an object of four inches or more, and the
last will take one of two inches in width.” In my specimen No. I, which is 1350 mm. long
(rather small for an adult), I find that the first gill-cleft (the one between the hyoid arch
and the first branchial arch) will admit the fingers and thumb of an entire hand; the
second, the four fingers as far as the palm; the third, the tips of four fingers; the fourth,
three fingers; the fifth, two large fingers; and the sixth, a thumb. These crude measure-
ments are sufficient to show the approximate size of the gill-clefts and the rapid decrease
in their size posteriorly.
Garman’s (1885.2) drawing (my Text-figure 77) of a gill-cleft and related structures
represents the fourth gill-opening on the right side. I have oriented the reproduction
of Garman’s figure with the dorsal side uppermost; this brings the anterior holobranch
to the right.
Each gill-arch of Chlamydoselachus affords attachment, distally, to one edge of
a crescentic plate, the gillsseptum. The framework of the gill-arches is supplied by the
cartilaginous branchial arches, while the gill-septa are strengthened by very slender
radially directed cartilaginous rods, the branchial rays. Each branchial ray begins in
contact with the cartilaginous branchial arch and extends to the extreme edge of the
gill-septum, where it may cause a slight projection of the overlying membrane. In places
the margin of the gill-septum is strengthened by a delicate extrabranchial cartilage.
On each side of a gillseptum there are long narrow primary folds, the gill-filaments,
extending in a radial direction from the base of the gill-sseptum toward its margin (Text-
figure 77; Text-figure 78, a.f. and p.f.). On each broad surface of a gill-fllament there are
The Anatomy of Chlamydoselachus 421
Text-figure 77.
The fourth gill-opening on the right side of a specimen of Chlamydoselachus anguineus, with the
gills spread apart to display the gill-filaments and branchial rays. The uppermost side of the
figure is dorsal, the right side anterior.
After Garman, 1885.2, Plate V.
Text-figure 78.
Radial section (x 4) of a gill of Chlamydoselachus, partly diagrammatic. The lines extending across
each filament indicate the sites of attachment of the lamellae on one surface of the filament. The
number of lamellae shown is approximately the actual number found in sections through the ventral
portion of the gill of the first branchial arch on the right side of Specimen No. I
ad.m., adductor branchialis muscle; a.f., anterior filament; af.br.a., afferent branchial artery; c., cartilage of the gill-arch;
c.m., superficial constrictor muscle of the gill-flap, continuous with the thinner interbranchial muscle of the gill-septum;
ef.br.a., efferent branchial arteriole; n., nerve; p.f., posterior filament; v., vein, presumably draining the small blood vessels
of the gill-septum.
Based on drawings of serial sections from two specimens in the American Museum of Natural History.
422 Bashford Dean Memorial Volume
transverse secondary folds or lamellae (Text-figures 78, 79, 80 Im.) too small for ordinary
observation. Goodrich (1930) and some others apply the term lamella to the structure
that I have called a filament, and designate as “secondary lamellae” the small leaf-like
folds that I have called simply lamellae. In my specimens, the distal end of a gill filament
is free for a distance of from 3 to 8 mm.; the gill-filaments never reach the distal edge of
the septum, but leave a smooth outer portion (from one-fourth to one-half of the entire
surface of the septum) constituting the gillflap or gill fold. Successive gill-flaps overlap
like the shingles on a roof. In addition to affording protection to the delicate gills,
they function as respiratory valves.
Sections showing filaments and lamellae of
a gill of Chlamydoselachus.
Text-figure 79. Portion of a section (x 12)
through the ventral part of the gill of the
fourth arch on the right side, cut trans-
versely to the filaments.
a.br., afferent branchial arteriole; e.br., efferent branchial
arteriole.
Drawn from a section of a gill from a specimen lent by
Dr. E. Grace White.
Textfigure 80. Outline of a portion of
a section (x 36) taken lengthwise of a gill-
filament, in the ventral part of the gill of
the first arch on the right side. The upper
end of the figure is distal.
A a., arteriole; Im., lamella.
“BS, de Drawn from a specimen in the American Museum of
figure 79. Text-figure 80. Natural History.
All the gill-flaments between two successive gill-clefts, together with the structures
supporting these gill-filaments, constitute a holobranch or entire gill. One of these is
shown, in a radial section cutting lengthwise of the filaments, in Text-figure 78. The
filaments on one side of a gillsseptum constitute a demibranch or half-gill. There is
a demibranch on both sides of each gill-cleft of Chlamydoselachus, excepting the posterior
side of the sixth or last gill-slit. In my specimens, as in Garman’s figure, the filaments on
the anterior side of a gill cleft are always longer than those on the posterior side. In
other words, the filaments of a posterior demibranch (posterior with reference to the
septum, not to the gill-cleft) are always longer than those of the anterior demibranch of the
same gill. Further, the filaments on both sides of the first gill-cleft are distinctly shorter
than those in corresponding positions with reference to the other gill-clefts. Since the
close-set filaments, all bearing numerous lamellae, of each demibranch are distributed
along the entire length of each gill and extend, on the average, considerably more than
halfway from the base of the septum to its free edge, it is apparent that the respiratory
The Anatomy of Chlamydoselachus 423
surface is very large—perhaps larger, in proportion to body size, than in most elasmo-
branchs. The blood vessels of the gills are described in the section on the blood-vascular
system, but it may be noted here that, thin as they are, the lamellae nevertheless contain
exceedingly rich capillary plexuses.
The general plan of a gill of Chlamydoselachus is much like that of Heptanchus (Text-
figure 81, which should be compared with Text-figure 78). Indeed, so far as the gills
of elasmobranchs have been studied, there is a considerable degree of uniformity in their
structure throughout the group.
From my observations I conclude that the gills of Chlamydoselachus are of the usual
elasmobranch type. In proportion to body size, the gill-clefts are unusually long (Text-
figure 4); they are separated by very slender branchial arches. The widely-distensible
ibd.
Text-figure 81.
Section, cutting parallel to branchial filaments, through second holobranch of Heptanchus maculatus.
ad., adductor muscle; af., third afferent artery; b.r., branchial ray cut short; csd., fourth dorsal constrictor muscle; eb., epi-
branchial segment of cartilaginous branchial arch; efc.4-5, fourth and fifth efferent collector arteries; ex.b., extrabranchial
cartilage; fl.a., anterior filament; fl.p., posterior filament; ib.d., dorsal interbranchial muscle; n., posterior division of the
branchial nerve.
After Daniel, 1934, Fig. 143.
pharynx is adapted for the rapid expulsion of a large volume of water through the gill-
clefts. This, in connection with the large respiratory surface afforded by the gill flaments
and particularly by their lamellae, makes an efficient mechanism for aerating the blood.
A discussion of the question as to the phylogenetic significance of the unusually
large number of gill-clefts and gill-arches in Chlamydoselachus and the notidanids would
lead us too far afield. Considerable data regarding the number of gill-clefts, from Amphiox-
us through the cyclostomes and fishes to the amphibian Cryptobranchus, is presented by
Corrington (1930, pp. 246-251), together with a discussion of the subject from an evolu-
tionary point of view.
THE SPIRACLES
The spiracles of elasmobranchs derive special interest from the fact that they arise
through modifications of a primitive first pair of gill-slits (Text-figure 62, p. 388) which, in
mammals, are represented by Eustachian tubes, tympanic cavities and external auditory
meatuses. In elasmobranchs the modifications are almost entirely concerned with the
regulation of the respiratory current, but the anatomical relations of certain parts presage
their use in connection with organs of hearing.
424 Bashford Dean Memorial Volume
The following description of the spiracles of Chlamydoselachus is based on my four
adult specimens, numbered I to IV respectively, of which the first three were dissected
by me and the fourth was studied without dissection.
The external spiracular apertures are ordinarily very small (Text-figures 70, p. 396;
and 124, p. 489). With one exception to be described presently, they are mere slits,
from 1 to3 mm. long. In my four specimens each aperture is situated in line with the
- =
a
= = SS
yy, = ———— eee
= ———
(14 Ws =
> LUlilt ————_—_—_ nS
Text-figure 82.
Left internal spiracular aperture and cavity (x 1.5) of Chlamydoselachus. The boundaries
of the cranium, hyomandibular, palatoquadrate, caecum and spiracular canal are indicated
by broken lines.
c.1, caecum; cr., cranium; hm., hyomandibular cartilage; i.s.c., internal spiracular aperture and cavity; I.p.i.,
ligamentum postspiraculare inferior; p.g., palatoquadrate cartilage (upper jaw); s.c., spiracular canal.
Drawn from specimen No. I in the collection of the American Museum of Natural History.
spiracular division of the sensory canal system (Text-figure 124, p. 489), about 8 mm.
from its anterodorsal end. In each case, the direction of the long axis of the slit-like
aperture coincides with that of the laterosensory canal. The lengths of the apertures in
our four specimens are as follows: No. I, 3 mm. on each side; No. II, 2 mm. on the right
side and 7 mm. on the left; No. III, 2 mm. on the right side and 1 mm. on the left; No.
IV, 3 mm. on the right side and 2 mm. on the left. The exceptionally large aperture on
the left side of No. Il is not a slit, but an elliptical opening fully three millimeters wide.
The unusually small opening on the left side of No. III could not be found until a bristle
had been inserted by way of the internal opening. It was overlooked entirely by Gudger
and Smith (1933) who also failed to identify as a spiracular opening the exceptionally
large aperture on the left side of No. II, mistaking it for a perforation made by a hook.
Each internal spiracular aperture or cavity (i.s.c.) is situated, in series with the gill
slits, between the hyomandibular cartilage and the palatoquadrate (Text-figure 82,
The Anatomy of Chlamydoselachus 425
hm., pg.). In my four specimens these openings are very much alike. They measure about
20 to 25 mm. long and are about 12 mm. wide when the pharynx is fully expanded. Thus
each internal spiracular aperture (i.s.c.) is large enough to admit a small finger. Its
posteromedial and anterolateral margins are well defined; they converge toward the
cranium and, when the pharynx is expanded, have the form of a furcula or ““wishbone.””
The posteromedial margin is formed by a prominent ridge where a fold of the mucous
membrane overlies a ligament (ligamentum postspiraculare inferior) extending along the
ventral surface of the hyomandibular cartilage and connecting it with the cranium. The
anterolateral margin is formed by a valve-like fold or flap of the mucous membrane.
There is no very definite ventrolateral margin, for here the inner surface of the pharynx
slopes gradually into the spiracular cavity. This side lies toward the palatoquadrate.
When the pharynx contracts, the posteromedial and anterolateral margins of the internal
spiracular aperture approximate until the opening is reduced to a mere slit compressed
between the hyomandibular and palatoquadrate cartilages. No doubt the opening may
be completely closed by the contraction of the pharynx, but this can occur only after
most of the water has been expelled from the pharynx.
Each internal spiracular aperture leads into a broad cavity or sac, the internal
spiracular cavity (Text-figure 82, i.s.c.), which is no wider than its internal opening and
is about 7 mm. deep in its deepest portion. The roof of this cavity lies in close proximity
to the integument. By palpation I found that the overlying plate of tissues, covering
not only the deeper portion of the cavity but also its sloping side toward the palato-
quadrate (Text-figure 82, p.q.), is decidedly thin. Evidently, it comprises little more than
integument and mucous membrane which come almost into apposition. In its structure
and in some of its relations this plate or membrane bears considerable resemblance to
the tympanic membrane of an amphibian. However, this membrane is evidently not
homologous with the structure described by Howes (1883) as the tympanic membrane
in Raja. Forming the anteromedial end of the internal spiracular cavity, beneath a flap
of mucous membrane, there is a pocket or caecum (c.1) which extends alongside the
hyomandibular in an anteromedial direction for a distance of about 10 mm. Its distal
end usually comes into contact with the auditory capsule of the cranium—a relation
which is most interesting when we compare the internal spiracular cavity of Chlamy-
doselachus with the tympanic cavity of higher vertebrates. In three instances, I found
in this caecum a large gelatinous mass, almost cartilaginous in consistency, which was
easily removed.
Before proceeding with the further description of the spiracle in my specimens
I quote the following from Goodey (1910.1, p. 550), who appears to be the only author
who has given any special attention to the spiracles of Chlamydoselachus:
On removing the skin [of Chlamydoselachus] and carefully dissecting away the under-
lying spongy cutis which covers the jaw muscles, it is seen that the lumen of the spiracle
passes down into the oral cavity between the hyomandibular and the mandibular [sic]
cartilages. Just inside the external opening, the cavity becomes enlarged and a short caecal
426 Bashford Dean Memorial Volume
diverticulum is given off anteriorly. This is overlaid by the levator maxillae muscle. . .
The caecum extends as far forward as the anterior knob of the proximal end of the hyoman-
dibular, which projects from the articular depression on the auditory capsule. It is not attached
to the hyomandibular, but is separated from it by the hyoidean branch of the seventh nerve,
which passes just internal and ventral to it. In all probability it is homologous with the
more extensive caeca mentioned by Ridewood (1896) which have been described in other
selachians by Muller and Van Bemmelen. In Scyllium, for example, the caecum extends
inwards over the hyomandibular and becomes firmly attached to the wall of the auditory
capsule, being in some way concerned with the function of hearing. A similar caecum is
found in Heptanchus, so that here we have another point in which Chlamydoselachus differs
from this member of the Notidanidae.
Text-figure 83.
Anterolateral wall of the left pseu-
dobranchial chamber and peripheral
wall of the spiracular canal (x 3)
of Chlamydoselachus, represented
in one plane.
p.f., pseudobranchial filament; s.c., spi-
racular canal.
Drawn from specimen No. I in the col-
lection of the American Museum of
Natural History.
Along the posteromedial side of the deeper portion of the internal spiracular cavity,
close to the hyomandibular, there is a narrow cleft with tumid lips, about 13 mm. long
and 5 mm. deep. This cleft (solidly black in Text-figure 82) is the pseudobranchial
chamber. The anterolateral lip is decidedly serrate, the posteromedial lip is slightly
serrate. The pseudobranchial chamber will be further described presently.
There is some variation in the manner in which the pseudobranchial chamber com:
municates with the external spiracular aperture. In specimen No. I, on the left side,
a bristle inserted into the pseudobranchial chamber, anywhere along its length, passes
posteromedially through a slit-like aperture into the spiracular canal (s.c. in Text-figures
82 and 83) which is compressed between the hyomandibular and the integument. The
spiracular canal becomes narrower as it approaches the external spiracular aperture. On
the right side, the pseudobranchial chamber communicates with the narrow spiracular
canal only by way of a small round opening situated at the posterolateral end of the
pseudobranchial chamber. In specimen No. I], on the left side, the external spiracular
aperture is exceptionally large and leads directly into the pseudobranchial chamber.
On the right side, the spiracular canal is like that on the left side of No. I. In specimen
No. IJ, which has unusually small external spiracular apertures, each pseudobranchial
chamber opens into the slender spiracular canal by means of a very small aperture situated
as it is on the right side of No. I. Thus I find, in my specimens, decided differences in
the size of the spiracular canal in the region where it communicates with the pseudo-
The Anatomy of Chlamydoselachus 427
branchial chamber: and in one case, which I regard as anomalous since the external
spiracular opening is very much larger than the others, the spiracular canal is absent.
In specimen No. I a bristle inserted into either external spiracular opening passes
anterolaterally, within the spiracular canal, to enter the pseudobranchial chamber. The
distance from the external spiracular aperture to the pseudobranchial chamber is about
10 mm., on each side. In specimen No. II, on the right side, a bristle inserted into the
spiracular canal by way of the external spiracular aperture travels about the same distance
and in a similar direction, before reaching the pseudobranchial chamber. In specimen
No. III, on either side, only a very slender bristle could be inserted by way of the ex-
ternal spiracular aperture, and this passed directly forward for a distance of about 5 mm.
before entering the pseudobranchial cavity. By dissection I have opened the spiracular
canals of specimens I, II, and III without finding anything of interest save a confirma-
tion of my description based on exploration with a bristle. Their walls are smooth.
The spiracular canal always lies just beneath the integument. Thus the external
spiracular aperture is bordered, on the side toward the canal, by a somewhat flexible
lip. In cases where the external opening is large enough to allow the passage of an
appreciable amount of water, this lip may function as a valve preventing the intake of
water through the spiracle while the pharynx is expanding. In my four preserved speci-
mens the entire spiracular canal is very much flattened, since it is compressed between
the hyomandibular cartilage and the integument.
In the free-swimming sharks, the spiracles are not so highly specialized for purposes
of respiration as in the skates and rays, which are bottom-dwelling forms. Concerning
the function of the spiracles, Daniel (1934, p. 156) writes as follows:
In the free-swimming sharks the current enters the mouth, from which it passes into
the pharynx and into the gill-pockets, the external clefts, including the spiracle, at the same
time remaining closed. The mouth then closes, the external clefts open, and the water is
forced out.
In the rays, which spend most of their time at the bottom and hence often in mud or
sand, there is an interesting change in the direction of the current. In these the greater part
of the current enters through the [large] spiracles and but little through the mouth. The
valves of the spiracles then close and the water is forced out ventrally through the external
branchial clefts. At the expulsion of the water the mouth does not entirely close, but only
a little of the water is able to gain exit through it because of valves which are located on its
roof and floor.
In Squatina, a bottom-dwelling shark, the respiratory current is known to enter
through the spiracles (Darbishire, 1907), though not exclusively (Daniel, 1934). From
my observations on the structure of the spiracle in Chlamydoselachus it is obvious that
this organ normally functions as in the free-swimming sharks and not as in Squatina.
From the small size of the external spiracular openings in Chlamydoselachus it is evident
that very little water passes through them.
428 Bashford Dean Memorial Volume
In elasmobranchs the spiracle ordinarily differs from the gill-slits in never possessing
gill-filaments, though it often has traces of these as a few small folds of the lining of its
anterior wall, which constitute the pseudobranch or mandibular gill. Allis (1923, p.
169) mentions pseudobranchial filaments in the “‘spiracular canal” of Chlamydoselachus,
but does not describe them. Goodey (1910.1, p. 550) writes of his specimens of Chlamy-
doselachus: ‘The pseudobranch in each spiracle consists of about ten short ridges,
which lie on the anterior outer wall just inside the external aperture. In the Noti-
danidae the pseudobranchs are said to be better developed than in any of the [other]
selachians, so that in this respect we find Chlamydoselachus presenting a small difference
from’ Heptanchus and Hexanchus.”
In my specimens I have distinguished a special chamber communicating with the
internal spiracular cavity (i.s.c.) on the one hand and the spiracular canal (s.c.) on the
other, which I call the pseudobranchial chamber (Text-figures 82 and 83). This chamber
presents for examination two surfaces, anterolateral and posteromedial respectively.
In specimen No. I each surface is about 13 mm. long (measured on the side toward the
internal spiracular cavity) and 5 mm. wide (measured from the internal spiracular cavity
to the beginning of the spiracular canal). Toward the internal spiracular cavity each
of these surfaces is bounded by a distinct ridge or lip, decidedly serrate in the case of the
anterolateral lip, only slightly so in the case of the posteromedial lip. The peripheral
boundary is not so well defined, save in those cases where the two surfaces meet on the
side toward the integument, leaving only a small round aperture leading from the postero-
lateral end of the pseudobranchial chamber into the spiracular canal. In cases where
the passage into the spiracular canal is large (as shown in Text-figures 82 and 83) the
boundary between this chamber and the spiracular canal may be defined as the line where
an abrupt change in direction occurs—for the pseudobranchial chamber lies along the
anterolateral surface of the hyomandibular, the spiracular canal along its peripheral
surface.
On the anterolateral wall or surface of the pseudobranchial chamber, the pseudo-
branchial filaments (Text-figure 83, p.f.) begin at regular intervals along the serrate lip
and extend peripherally for a distance varying from 2 to 5 mm. The serrations corre-
spond to the filaments—that is, the projections, which appear tooth-like when the lips of
the pseudobranchial chamber are approximated, are seen to be the proximal ends of the
folds or filaments when the chamber is opened to view. The pseudobranchial filaments
are little more than mere ridges; the height of these filaments seldom exceeds 1 mm.
and is never more than 1.5mm. The longest filaments are usually those near the middle
of the row. Some of the filaments—particularly those of the left pseudobranchial chamber
of specimen No. II, which has the largest filaments—are free at their peripheral ends,
where they project as finger-shaped structures as in the case of ordinary gill-filaments.
The number of filaments composing each pseudobranch varies from eight to sixteen.
So far as I know, a pseudobranch on the posteromedial surface of the pseudobranchial
chamber has never been described in any elasmobranch. Nevertheless I find, on this
The Anatomy of Chlamydoselachus 429
surface in some spiracles of my specimens, structures which may be vestiges of gill
filaments. These structures are low ridges, soft when palpated but not disappearing
entirely when the mucous membrane is stretched at right angles to their long axes. They
are spaced regularly, like gillfilaments. In number, position, length and direction they
resemble the pseudobranchial filaments on the opposite side of the pseudobranchial
chamber, but they are usually broader and are never so high. I suspect that if fresh
specimens were available, the presence of vestigial gill-filaments on the posteromedial
wall of the pseudobranchial chamber could be conclusively demonstrated.
A pit or depression representing the ventral end of a primitive gill-cleft extending
between the hyoid and mandibular arches has been described by Ridewood (1896) in
Galeus, Carcharias, Zygaena, Triacis and Chiloscyllium. It is faintly marked in Mus-
telus, but is absent in Scyllium, Notidanus and Acanthias. Concerning this pit or de-
pression Ridewood writes as follows:
If a line be drawn joining the lower ends of the pharyngeal apertures of the branchial
clefts, it will pass through the lower or anterior extremity of the pit, just as a curved line
joining the upper ends of the branchial clefts will, if produced, pass through the inner or supe-
rior edge of the pharyngeal aperture of the spiracle. It is universally admitted that the
spiracle of sharks represents only the upper part of the hyoid cleft, the middle and lower
portions being obliterated. Hence, in this depression of the mucous membrane, is a structure
which, in complete absence of evidence to the contrary, may be regarded as the internal or
pharyngeal portion of the lower half of the hyoid cleft.
In my four adult specimens of Chlamydoselachus I found, on each side of the floor
of the pharynx, between the ceratohyoid and mandibular cartilages and directly ventral
to the internal spiracular aperture, a large opening (Text-figure 84, v.g.c.) leading into
Text-figure 84.
Left internal spiracular aperture and vestigial
gill-cleft (x 0.86) of Chlamydoselachus in their
relation to each other and to the adjoining
cartilages.
br.c.1, first gill-cleft, showing the demibranch attached to
the hyomandibular and ceratohyoid cartilages; br.c.2-3,
second and third gill-clefts; c.1, caecum of the internal
spiracular cavity; c.2, caecum of the vestigial gill-cleft;
ch, ceratohyoid cartilage; cr, cranium; i.s.c., internal
spiracular aperture and cavity; hm, hyomandibular
cartilage; |.p.i., ligamentum postspiraculare inferior;
m, mandible or Meckel’s cartilage; pq, palatoquadrate:
s.c., spiracular canal; v.g.c., vestigial gill-cleft.
Drawn from specimen No. I in the collection of the
American Museum of Natural History.
430 Bashford Dean Memorial Volume
a pocket or caecum. This, like the pit or depression mentioned by Ridewood, is evidently
a vestige of the ventral end of a primitive gill-cleft. Although Ridewood was careful to
describe the relations of the pit or depression studied by him, he does not give any descrip-
tion of the pit itself further than that implied in the terms used. | infer that the pit or
depression examined by Ridewood is so simple that it does not need any further descrip-
tion. In Chlamydoselachus the opening is in series with the ventral ends of the branchial
clefts. In my four specimens it is from 8 to 15 mm. long and is bordered on the lateral
side (toward the mandible) by a crescentic valve-like flap or fold of the mucous membrane.
The medial side has no definite boundary. The opening leads into a shallow cavity or
caecum (Text-figure 84, c.2) extending beneath the flap posteriorly and laterally for
a distance of from 3 to 5 mm., anteriorly for a distance of from 5 to 20 mm. Its average
extension anteriorly is about 12 mm., as shown in the figure. The structure and relations
of this cavity leave no doubt that it is a persistent ventral portion of a primitive gill-
cleft originally continuous with the dorsal portion now represented by the spiracle.
This primitive gill-cleft was bordered on the anterior side by the elements comprising
the jaw-cartilages, on the posterior side by the hyoid arch represented by the ceratohyoid
and the hyomandibular cartilages.
Since writing the preceding paragraph and preparing the accompanying illustrations,
(Text-figures 82 and 84), I have found in the midst of a description by Allis (1916, pp.
110-111) of the mandibular artery of Chlamydoselachus, the following account of a some-
what similar pocket in the lining of the oropharyngeal cavity of his specimen:
This latter branch [of the arteria mandibularis], on both sides of the head of this speci-
men, passes immediately anterior to a relatively deep tubular pocket, or recess, of the lining
membrane of the mouth cavity which, beginning slightly posterior to the angle of the gape,
extends dorsoposteriorly toward the quadrato-mandibular articulation. This pocket lies
along the external surface of the hind end of the palatoquadrate, between that cartilage and
those fibers of the musculus adductor mandibulae that pass uninterruptedly from the upper
to the lower jaw. Posteriorly it ends blindly, its blind end being attached to ligamentous
tissues which, continuing on in the line prolonged of the pocket, are attached to the hind
(distal) end of the palatoquadrate. The pocket thus lies morphologically anterior to the
palatoquadrate, in the relation to that cartilage that a persisting remnant either of the mandib-
ular cleft or of a premandibular cleft would have, and its position, posterior to the musculus
mandibulae, is not unfavorable to its being a remnant of either of those clefts, for the adductor
muscle, if it be derived from the superficial constrictor of the mandibular arch, could readily,
when it slipped from the external (actually posterior) edge of the arch on to its anterior
(actually lateral) surface, have acquired a position superficial, and hence morphologically
anterior, to the pocket. A branch of the artery is sent posteriorly, on either side of the
pocket, to the adductor muscle.
It is evident, upon comparing this description with Text-figure 84, that the pocket
described by Allis does not have the same anatomical relations as the one described and
figured by me.
The Anatomy of Chlamydoselachus 431
THE UROGENITAL SYSTEM
In Chlamydoselachus, as in other vertebrates, the urogenital system comprises two
functionally distinct parts, the excretory system and the reproductive system; but these
are so closely related developmentally and anatomically, especially in the male, that it
is often convenient to refer to them collectively.
UROGENITAL SYSTEM OF THE FEMALE
Since the literature on the urogenital system of Chlamydoselachus is very meager,
the following account is based mainly on my own observations and drawings which were
made from four large specimens: Nos. I, II and III collected in Japan by Dr. Bashford
Dean and now in the American Museum of Natural History, and another specimen
(No. IV) kindly lent by Dr. E. Grace White. All four specimens are females. References
to the work of other investigators are made throughout the text. Brohmer’s (1908)
account of the excretory system of an embryo of Chlamydoselachus deals with an early
stage and need not be considered here.
UROGENITAL SINUS IN THE FEMALE
In some elasmobranchs the expression“urogenital sinus” is hardly applicable to the
female, but in the case of Chlamydoselachus I can see no reason for avoiding the use of this
convenient term. In all my specimens the urogenital portion of the cloaca is quite plainly
marked off from the rectal portion, though the distinction is most clear-cut in the decidedly
immature specimen.
In this specimen (No. IV) a small aperture (Text-figure 85, ug.s.), situated on the
dorsal surface of the rectal portion of the cloaca, leads into the urogenital sinus which
extends in an anterodorsal direction for a distance of about 13 mm. The urogenital sinus
must be examined by dissection. It is about 10 mm. wide, but its opening into the rectal
portion of the cloaca has a width of only 5mm. On each side of the sinus, near its anterior
end, there is an opening from the uterine portion of an oviduct. The urinary papilla is
a longitudinal fluted ridge, free at its posterior end, situated on the dorsal surface of the
sinus a little to the left of the median line. The urethral aperture, a narrow slit not more
than 3 mm. long, is located near the center of the papilla. No urethral orifice could be
found on the right side of this specimen.
In specimen No. III, which is nearly mature, the urogenital sinus (shown without
a label in Text-figure 86) is still sharply marked off from the rectal portion of the cloaca,
though its opening is much larger than in specimen No. IV. The orifices of the uteri
are not shown in the figure since they open into the anterior portion of the urogenital
sinus, which lies dorsal to the rectal cloaca. The opening of the right uterus is large
enough to admit a finger; the left is much smaller. The urinary papilla is a broad ridge,
not well defined, on the dorsal surface of the urogenital sinus. The single urethral
orifice is a round pore (ur.p.), readily admitting a probe. It is situated near the center
of the dorsal surface of the urogenital sinus, but a trifle to the left.
432 Bashford Dean Memorial Volume
In specimen No. I, which is fully mature, the urogenital sinus (Text-figure 87) is
still slightly constricted where it joins the rectal portion of the cloaca, but the openings
of the uteri are readily visible and are indicated by line-shading in the figure. The right
uterus has a much larger opening than the left. There are two urethral pores (ur.p.),
right and left, and these are situated close together near the posterior end of the dorsal
Urogenital system of the female Chlamydosel-
achus, ventral views, one-fifth natural size.
Text-figure 85. Urogenital organs of a specimen
1398 mm. long. The excretory ducts are
concealed by the oviducts.
ab.p., abdominal pore; m., mesonephros; ovd., oviduct;
ovy., ovary; r.cl., rectal portion of the cloaca; ug.s., open-
ing from the urogenital sinus; v.l., ventral ligament of
the oviduct.
Drawn from specimen No. IV in the American Museum
of Natural History.
Text-figure 86. Urogenital organs of a specimen
1550 mm. long. The shell glands and the
adjacent portions of the oviducts are displaced
laterally, and the excretory ducts are not shown.
ab.p., abdominal pore; m., mesonephros; ovd., oviduct;
ovy., ovary; r.cl., rectal portion of the cloaca; s.g., shell
gland; ur.p., urethral pore; ut., uterus; v.!., ventral ligament
of the oviduct.
Drawn from specimen No. III in the American Museum
of Natural History.
rch.’
26.p---YOs
Text-figure 85. Text-figure 86.
surface of the urogenital sinus. The right urethral aperture is decidedly smaller than the
left and is situated a little further posteriorly. There is no urinary papilla.
In specimen No. II, which is fully mature, almost the entire urogenital sinus (Text-
figure 88) seems built around the very large opening of the right uterus, indicated by line-
shading in the figure. In the hardened condition of the material, this opening is still
large enough to admit a thumb. The opening of the left uterus is much smaller. There
are two urethral orifices, right and left, situated about 4 mm. apart near the center of the
dorsal surface of the urogenital sinus. The right urethral aperture (ur.p.) is somewhat
The Anatomy of Chlamydoselachus 433
smaller than the left. There is no urinary papilla. The rectal portion of the cloaca is
very short.
A ventral view of the cloaca of Garman’s (1885.2) adult female specimen of Chlamy-
doselachus is shown in his Pl. XII, reproduced here as Text-figure 89. There is no line
of demarcation between urogenital and rectal portions of the cloaca (cl.). There is only
Urogenital system of the female Chlamydo-
selachus, ventral views, one-fifth natural size.
The shell-glands and the adjoining portions of
the oviducts are displaced laterally.
Text-figure 87. Urogenital organs of a speci-
men 1350 mm. long. The right uterus and
ovary are incomplete.
TE eee
rr
ab.p., right abdominal pore (the left is closed superfici-
ally); c.t., collecting tubule; m., mesonephros; mes.d.,
mesonephric duct; mso., mesovarium; ovd., oviduct; ovy.,
ovary; r.cl., rectal portion of the cloaca; s.g., shell gland;
ur.p., urethral pores; ut., uterus; v.I., ventral ligament
of the oviduct.
Drawn from specimen No. I in the American Museum
of Natural History.
Text-figure 88. Urogenital organs of a speci-
men 1485 mm. long. A segment has been
excised from the right uterus, and the right
ovary is incomplete. The excretory ducts are
not shown.
ab.p., abdominal pore; m., mesonephros; ovd., oviduct;
ovy., Ovary; 7., rectum; s.g., shell gland; ur.p., urethral
pores; ut., uterus; v.l., ventral ligament of the oviduct. 7
Drawn from specimen No. II in the American Museum Ar
of Natural History unp. el
\ 26 p,
Text-figure 87. Text-figure 88.
one urethral aperture; this (u.a.) is rather large and its position is median. Garman
states that “there is no appearance of a urethral papilla; the anterior border of the opening
is inflated into a flap or valve, which closes the opening against objects passing outward
through the cloaca, or better, which is made to close it by the object themselves.”
Hawkes (1907) has represented the cloaca of her female specimen of Chlamydoselachus
by a diagram which is reproduced as my Text-figure 90a. She notes that there are two
434 Bashford Dean Memorial Volume
small cloacal apertures (U.S.1) for the urinary sinuses (U.S.) of which only the one on
the left side is shown. These apertures are situated close to the median line near the
posterior border of the cloaca. She states further that in the female the rectal aperture
(R.) is displaced to the right. The opening of the right oviduct (R.Ov.) is much larger
than the left (L.Ov.), and appears to crowd the latter anteriorly. This, perhaps, explains
the displacement of the rectal opening to the right.
Text-figure 89.
Ventral view of cloaca, pelvis and pelvic fin cartilages of a female Chlamydoselachus.
ab.p., abdominal pores; bp., basipterygium; cl., cloaca; u.a., urethral aperture.
After Garman, 1885.2, Pl. XII.
ORGANS OF EXCRETION IN THE FEMALE
The organs of excretion in the female Chlamydoselachus consist of a pair of meso-
nephroi or functional kidneys, numerous collecting tubules, a pair of mesonephric ducts
or Wolffian ducts, and a pair of urinary sinuses or functional bladders which are formed
by the enlargement of the posterior portions of the mesonephric ducts. In each of my
four specimens, the two urinary sinuses are entirely separate structures.
Tue MesonepuHroi.—In my four female specimens, the mesonephroi are a pair of
slender flattened organs (m. in Text-figures 85 to 88) extending through about 87 per cent
of the total length of the body cavity (Tables Il and III). Posteriorly, the mesonephrot
begin dorsal to the posterior margin of the rectal portion of the cloaca, save in specimen
No. IV where they begin as far back as the urethral orifice. Thus the mesonephroi do
not begin at the extreme posterior limit of the body cavity, which extends farther caudad
dorsally than it does ventrally. Dorsally, the body cavity extends as far back as the ex-
ternal openings of the abdominal pores, which are situated ventrally. The members of
The Anatomy of Chlamydoselachus 435
a pair of mesonephroi are usually of equal length, but in specimen No. II (Text-figure 88)
the left mesonephros is shorter than the right. In most cases the mesonephroi thin
out so gradually at the anterior end that the anterior limit can be made out only after a
careful examination.
Text-figure 90.
Diagrammatic figures of the cloaca in female (A) and male (B) specimens
of Chlamydoselachus.
A.P., closed abdominal pore; BI., so-called bladder (urogenital sinus); L.Ov., left oviducal open-
ing; R., rectum; R.A.P., functional right abdominal pore; R.G., opening of rectal gland into
the rectum; R.Ov., right oviducal opening; R.S., seminal vesicle; Ug., urogenital opening;
Ur., opening of ureter into urogenital sinus; U.S., urinary sinus of female (one sinus is omitted
from the drawing); U.S.1, openings of urinary sinuses into the cloaca; V.D., vas deferens
(ductus deferens).
After Hawkes, 1907, second text-figure, p. 476.
In Table II are shown the lengths of the mesonephroi in my specimens, together
with the ‘over-all’ length of the body and the total length of the body cavity. In Table
III the ratios of length of mesonephros to body length and to length of the body cavity
are expressed in percentages. From an inspection of Text-figures 85 to 88 it will be seen
that specimen No. IV is sexually immature, No. II is nearly mature, while Nos. I and
I are fully mature. The variations shown in Tables II and III are too small to be signif-
TABLE II
Length in millimeters of the mesonephros of the female Chlamydoselachus compared with the total
length of its body and the entire length of its body cavity. The specimens are arranged in the order of
sexual maturity.
ashes
Specimen Number | IV. | Ill. | I Il. |
| | | |
fin TTT eh aa | li ee = al
Total Length of Body | 1398 | 1550 | 1350 | 1485
Length of Body Cavity 554 634 588 686
Length of Mesonephros__ | 486 554 | 518 605*
| |
*This applies to the right mesonephros only. In this specimen the left mesonephros is shorter; its
length is 541 millimeters.
436 Bashford Dean Memorial Volume
TABLE II.
Length of the mesonephros in proportion to the total body length and to the entire length of the body
cavity, in four female specimens of Chlamydoselachus, shown in percentages. The specimens are arranged
in the order of sexual maturity.
Specimen Number IV. I. | L UL.
Length of Mesonephros
A 35. 38.3 40.
Tage Peeyy Waa ool Doll 7
Length of Mesonephros
||. eetooerie ene Seer are 87.7 87.3 88.0 88.1*
| Length of Body Cavity | |
|
*Percentage computed from the right mesonephros only.
icant of either developmental or retrogressive changes. Therefore I conclude that there
is no appreciable change in the length of the mesonephros proportional to body length
or to the length of the body cavity, within the age limits represented by my specimens.
From dissections, one gets the impression that the mesonephroi originally extended
a little further forward, since vestiges of these organs appear in front of the unequivocal
portions represented in the figures. In any event, the length of the mesonephros in the
female Chlamydoselachus is remarkable. In many of the more highly differentiated
elasmobranchs (e.g., the skates) only the posterior portion of the female mesonephros
persists in the adult. In Chlamydoselachus, the presence of the mesonephros through-
out almost the entire length of the body cavity of the female must be accounted a
primitive character.
Throughout their entire extent, the mesonephroi lie against the dorsal body wall,
close to the median line. At their posterior ends they are actually united, but they
diverge a little anteriorly. Therefore, along the greater part of their course they lie
along the low ridge formed by the vertebral column, but at their anterior ends they
depart slightly from this ridge. In specimens IV, III and I, the mesonephroi lie almost
flat against the dorsal body wall; therefore in Text-figures 85, 86 and 87, which are drawn
from these specimens, the mesonephroi are shown very nearly in broad view. Variations
in the width of the mesonephroi are fairly well shown in these figures. In specimen No.
III, which has the largest mesonephroi, each mesonephros has a maximum width of 13 mm.
In specimen No. II (Text-figure 88), within the posterior half of the body cavity the
mesonephroi are approximated to such a degree that the surfaces ordinarily dorsal are
medial. Hence, in a ventral view, the mesonephroi are seen almost on edge, so that
their actual width is not fully represented in the figure. In the anterior half of the body
cavity of No. II, the mesonephroi gradually become flattened against the body wall as
they diverge anteriorly.
There is considerable variation in the extent of union of the mesonephroi at their
posterior ends. In specimen No. IV the two mesonephroi are united across the median
plane for a distance of about 80 mm. measured from their posterior ends; in No. IU,
The Anatomy of Chlamydoselachus 437
for a distance of 70 mm.; in No. I, for about 100 mm.; while in No. II they are united
for a distance of 296mm. In this respect, as in some others already noted, the mesonephroi
of specimen No. II are atypical.
In general, the mesonephroi are thickest at their posterior ends, where each meso-
nephros (considered as a separate entity) has a maximum thickness equal to about one-
third its width. Anteriorly, the mesonephroi become thinner very gradually. No. IV
is exceptional in that the caudal portion of each mesonephros, for a distance of 15 mm.
measured from its posterior end, is abruptly thicker than the part immediately in front
of it. This caudal portion has a thickness equal to about two-thirds its width.
Since the mesonephroi are entirely retroperitoneal, they come into actual contact
with the peritoneum only by their broad ventral or ventrolateral surfaces. Wherever
the mesonephroi are approximated, they lie close to the base of the dorsal mesentery,
which extends along the dorsal median line for the entire length of the body cavity.
The dorsal mesentery gives rise, laterally, to special mesenteries supporting the oviducal
organs and the ovaries; ventrally, to a continuous median mesentery supporting the
digestive tube excepting the posterior four-fifths of the valvular intestine and the entire
rectum. The mesenteries related to the mesonephroi and to the oviducal organs are
particularly important, since these mesenteries contain the collecting tubules and the
mesonephric ducts.
In order to investigate the microscopic structure of the mesonephros and the relations
of the right and left mesonephroi to each other, transverse serial sections were cut from
segments taken at intervals along the length of these organs in all my specimens. In
every case the material was found to be in very poor condition for histological study, but
mesonephric tubules and glomeruli were readily identified. In the region of union, the
two mesonephroi are sometimes connected by renal tissue, but more often by what
appears to be lymphoid tissue.
Since the mesonephroi are seldom, if ever, disturbed when newly-captured specimens
are eviscerated by fishermen, it seems strange that there is so little recorded concerning
them. Collett (1897) describes the mesonephroi of his large female specimen as follows:
“The kidneys were also very long, the right being the longer (length 780 mm.) and rather
flat, the left being more cylindrical, and of a length of 770 mm. Posteriorly, both kidneys
form a club-shaped, thickened, coalescent portion terminating somewhat abruptly toward
the anus. The length of the coalescent portion is 120 mm.” The only additional descrip-
tion of the “kidney” of Chlamydoselachus that I have found is that of Hawkes (1907, p.
477), which reads as follows:
The kidney in the female [Chlamydoselachus] is thin dorsoventrally and of irregular
breadth. It extends from the region of the oviducal gland to the end of the body cavity,
gradually widening as it passes backward in a sinuous line. The sinuosity is due to the
arrangement of some of the dorsal muscles. Cephalad to the kidney and apparently uncon-
nected with it, there is an irregular body (1.5 cm.) which extends somewhat beyond the end
of the abdominal cavity. This is probably the head kidney (pronephros?) which in the adult
has retained its position in the region to which the coelome extended in the embryo.
438 Bashford Dean Memorial Volume
In the absence of any statements to the contrary, it may be assumed that the “kidney”
of Hawkes’ specimen was a paired structure, and that the two, more or less separate,
members were of equal length. As already noted, in one of my specimens (and less
significantly in Collett’s large specimen) the left mesonephros is shorter than the right.
This does not necessarily mean a decrease in function of the left mesonephros, since
a shortening of the thin anterior end might readily be compensated by a hardly noticeable
increase in thickness posteriorly. A concentration of the adult female mesonephros into
a compact organ situated in the posterior part of the body cavity is characteristic of the
highly specialized elasmobranchs.
Concerning the mesonephroi of the female Heptanchus, Daniel (1934, p. 287) writes
as follows: “Each kidney extends as a narrow ribbon of tissue from the pericardio-
peritoneal septum posteriorly one-half the length of the body cavity; back of this it
broadens out and becomes much thicker so that the main mass of the tissue lies posterior
to the region of the superior mesenteric artery.” From an inspection of Daniel’s figures
it appears that the broadening of the posterior part of the “kidney” is rather abrupt, not
gradual as in the case of Chlamydoselachus. The assertion that the kidney of the female
Heptanchus extends from the pericardio-peritoneal septum is hardly understandable in
view of Daniel’s statement (p. 289) that the kidney of the male extends farther forward
than that of the female.
Tue Urinary Stnuses.—In specimen No. IV, which is immature, a probe inserted
through the urethral orifice passes in one direction (anterodorsally) only, for a distance
of about 10 mm. The slender cavity thus explored is the rudimentary left urinary sinus.
Its posterior half is imbedded in the thick dorsal wall of the urogenital sinus, while its
anterior half lies in a thick portion of the dorsal mesentery supporting the two uteri
which are joined by their medial walls for a distance of 50 mm. anterior to the urogenital
sinus. The left mesonephric duct, too small to be probed but clearly visible with a hand
lens, extends anteriorly from the left urinary sinus along the base of the dorsal mesentery
close to the left mesonephros. There is a right urinary sinus, of the same size as the left
and in a corresponding position. Anteriorly, it is continuous with the right mesonephric
duct which lies alongside the left; but I could not find any opening from the right urinary
sinus into the urogenital sinus, either by way of the urethral orifice which serves as an
outlet for the left mesonephric duct, or otherwise. The right urinary sinus was found
by dissection, using the right mesonephric duct asa guide. I could not find any aperture
connecting the two urinary sinuses, which are separated by a thick septum.
In specimen No. III the two urinary sinuses (Text-figure 914), right and left, lie
close to the median plane. The left urinary sinus extends 75 mm. anterior to the urethral
orifice. Near its posterior end this sinus is broad but shallow; its greatest width is
9mm. Fora distance of 25 mm. from the urethral orifice, the expanded posterior portion
of the left urinary sinus lies within the dorsal and left lateral wall of the urogenital sinus.
Here, only the medial border of the left urinary sinus comes into relation with the dorsal
mesentery which connects the urogenital sinus with the dorsal body wall and with the
The Anatomy of Chlamydoselachus 439
mesonephroi. Anteriorly, the left urinary sinus gradually diminishes in caliber as it
extends within the dorsal mesentery close to the uteri which are united by their medial
walls for a distance of 40 mm. in front of the urogenital sinus. At 75 mm. from the
urogenital orifice, the left urinary sinus tapers rather abruptly to become continuous with
the left mesonephric duct which extends forward in the dorsal mesentery. The right
urinary sinus is apparently cystic, and was found by dissection. It begins as far poste-
riorly as the left urinary sinus, but is only 60 mm. long and 8 mm. wide in its widest
portion. Its relations to the wall of the urogenital sinus and to the dorsal mesentery are
Text-figure 91.
Urinary sinuses (ventral views, three-
fifths natural size) of three female
specimens of Chlamydoselachus: A,
specimen No. III; B, No. I; C, No. II.
In order to show the correct propor-
tions, the outlines are drawn as if the
sinuses were spread in a horizontal
plane.
Drawn from specimens in the American
Museum of Natural History.
similar to those of the left urinary sinus. While the left urinary sinus readily admits
a probe by way of the urethral pore, and the probe continues into the left mesonephric
duct, no opening for the right urinary sinus could be found in any direction.
Specimen No. I has a pair of well-developed urinary sinuses (Text-figure 91s)
situated close to the median plane but lacking any direct communication with each other.
In this specimen the two uteri are united by their medial walls for a distance of 50 mm.
in front of the urinary sinuses, hence are supported, in this region, directly by the
dorsal mesentery. The relations of the urinary sinuses to the wall of the urogenital
sinus and to the dorsal mesentery are the same as in specimen No. III, save that here the
urinary sinus of the right side is confined to the dorsal mesentery. Each urinary sinus
connects posteriorly with its short urethral pore, through which it may be probed. The
urinary sinus of the left side is larger than the corresponding sinus of No. II; it is about
90 mm. long, and 10 mm. wide throughout more than half its length. The posterior end
narrows abruptly, the anterior end so gradually that its limit must be determined some-
what arbitrarily. The sinus is continuous anteriorly with the left mesonephric duct
which was probed more easily than that of No. III. The right urinary sinus is slightly
smaller than the left. It is 85 mm. long, and 8 mm. wide throughout its middle third;
440 Bashford Dean Memorial Volume
it tapers gradually both anteriorly and posteriorly. Anteriorly, the right urinary sinus
is continuous with the right mesonephric duct which was easily probed.
In Specimen No. II the urinary sinuses (Text-figure 91c) are well developed and are
situated close to the median plane. As in the other specimens, they are not united to
form a single functional bladder. Each urinary sinus connects posteriorly with a short
urethral pore, through which it may be probed. The two uteri are united by their medial
walls for a distance of 50 mm. in front of the urogenital sinus, and so have a common
dorsal mesentery. The relations of the urinary sinuses to the urogenital sinus and to the
Text-figure 92.
Longitudinal section through cloaca and right oviduct of Chlamydoselachus,
three-fourths natural size. The dorsal side is uppermost.
ab-p, abdominal pore; cl, cloaca; int, intestine; ov, oviduct; p, caecal pouch, or rectal gland; ua
urethral aperture.
After Garman, 1885.2, Fig. 2, pl. XIX.
2
dorsal mesentery are much the same as in specimen No. III. The left urinary sinus is
only 50 mm. long, but it is comparatively broad, having a maximum width of 10 mm.
The left mesonephric duct could not be probed. The right urinary sinus is about 100
mm. long. It has a maximum width of 7 mm., but there is an abrupt constriction in its
posterior third. In its anterior half it tapers very gradually to become continuous with
the right mesonephric duct, which was probed for a distance of 20 mm. in front of the
urinary sinus.
In the well-developed urinary sinuses of specimens III, I, and II, the direction of
greatest width is determined by the relations to the urogenital sinus and to the dorsal
mesentery. In most cases by far the greater portion of the urinary sinus is imbedded in
the dorsal mesentery, and the direction of greatest width of the sinus is therefore mainly
dorsoventral. In Text-figure 91 some liberties have been taken with the anatomical
relations in order to show the full width of the urinary sinuses.
The Anatomy of Chlamydoselachus 441
Garman (1885.2) states that in his (female) specimen of Chlamydoselachus the
“ureters” unite before reaching the cloaca, into which they empty by means of a single
aperture. From an inspection of his figure reproduced as my Text-figure 92, it appears
probable that the so-called ureters are large mesonephric ducts which unite before reaching
the single urethral opening. The fused portion may be considered a rudimentary urinary
sinus.
Concerning the urinary sinuses of Chlamydoselachus, Hawkes (1907, p. 477), whose
observations were apparently made on a single specimen, writes:
Each [urethral] aperture passes into an expanded chamber [U.S., my Text-figure 90a,
after Hawkes] with laminated walls, the lumen of which has a diameter of 5 mm. in the
cloacal region. The first portion of the sinus is imbedded in the thick cloacal walls. Each
sinus extends forward for a distance of 6 cm. beyond the cloaca along the inner side of the
kidney, but in front of this point it lies near the oviduct, at a distance from the kidney varying
from 1 to 2 cm.
A survey of the specimens described to date indicates that paired urinary sinuses,
opening into the urogenital sinus by separate urethral apertures, are typical for the female
Chlamydoselachus. Nevertheless, there is marked variability. The rudimentary median
urinary sinus, or posterior fused portion of the mesonephric ducts, described by Garman,
is anomalous. It illustrates one method by which a single median bladder, opening by
a single urethral aperture, might be evolved. In my specimens, I find two instances
(Text-figures 91a and B) where the right urinary sinus is smaller than the left, and one
instance (Text-figure 91c) where the right urinary sinus is irregular in shape. In two
instances (specimens IV and III) a right urethral aperture could not be found, while in
two others (Nos. I and II) the right urethral aperture is smaller than the left. In No. III
no connection of the right urinary sinus with a mesonephric duct could be found. To
offset these deficiencies of the right urinary sinus and its openings there is but one instance
of similar deficiency on the left side: in No. Il a probe could not be passed from the left
urinary sinus into the left mesonephric duct, though the latter is of normal size. It is
evident that the urinary sinus and also the urethral pore of the right side are much more
likely to be defective. That genetic factors are involved is probable from the condition
in specimen No. IV, which is quite immature, and in No. II, which is not fully mature.
In Heptanchus maculatus (Daniel, 1934) there is ordinarily a single median urinary
sinus, but in one specimen two urinary sinuses, right and left respectively, were found.
I have been unable to find any other instances, except in Chlamydoselachus, of a pair of
urinary sinuses opening separately into the urogenital sinus of an elasmobranch. In the
Myxinidae, the mesonephric ducts are said (Sedgwick, 1905) to open separately into the
urogenital sinus, but in Petromyzon these ducts join to discharge their fluid through
a single pore. In vertebrate embryos, the mesonephric ducts open separately. The
condition found in Chlamydoselachus is probably primitive in a phylogenetic sense,
but may be due to arrested development.
442 Bashford Dean Memorial Volume
MaesonePuRic Ducts AND CoLLecTING TusBuLes.—In specimen No. IV, which is
immature, the mesonephric ducts are so slender that they are barely visible to the naked
eye, but with the aid of a dissecting lens they were easily recognized. They were identi-
fied also in transverse serial sections of the urogenital system taken at distances of ap-
proximately 25 mm., 140 mm. and 400 mm. from the posterior ends of the mesonephroi.
In all three regions the mesonephric ducts lie side by side—at 25 mm. and 140 mm.,
close together within the dorsal mesentery; and at 400 mm., some little distance apart,
within the very narrow special mesenteries supporting the oviducts. The mesonephric
ducts are of equal size. Collecting tubules were not positively identified.
In specimen No. III the left mesonephric duct was probed for a distance of 25 mm.
from the left urinary sinus, and was bristled for an equal distance further. Throughout
this posterior 50 mm. of its course, it runs in the narrow dorsal mesentery. Due, perhaps,
to the poor preservation of the material, the duct could not be satisfactorily traced
further. No duct connected with the right urinary sinus could be found by dissection.
Collecting tubules could not be identified. A segment of the dorsal mesentery taken
about 100 mm. in front of the urethral pore was sectioned transversely. The sections
show two mesonephric ducts, side by side, but of unequal size. The right duct is the
smaller, and in places is almost obliterated.
Of my four specimens, No. I (Text-figures 87 and 93) is most favorable for the study
of the duct system. The left mesonephric duct (mes.d.) was easily probed, by way of the
left urinary sinus, for a distance of about 80 mm. in front of the urinary sinus. Through
out this distance it runs in the dorsal mesentery; but just where the probe fails to
penetrate, the duct leaves the dorsal mesentery to enter the special mesentery supporting
the left uterus. In its further course the duct is quite conspicuous and it was easily
traced almost to the anterior end of the mesonephros. In the anterior third of the body
cavity, the duct again courses in the basal portion of the dorsal mesentery. The right
mesonephric duct has a similar distribution. It was probed for 80 mm. from the right
urinary sinus, but in general it is not quite so well developed as the left duct. Where
the two ducts course together in the dorsal mesentery they do not lie side by side. Poste-
riorly, the left duct is immediately dorsal to the right; anteriorly, the left duct is some
little distance ventral to the right. Collecting tubules (c.t.) entering the right duct are
about as numerous as those entering the left duct. All the tubules incline forward as
they course ventrad from the mesonephroi to the ducts. In the dorsal mesentery the
tubules leading to right and left ducts respectively are roughly alternate in position.
Since the mesonephroi extend posteriorly much farther than the mesonephric ducts,
the question arises whether any collecting tubules from the posterior end of a mesonephros
enter the urinary sinus directly instead of by way of the mesonephric ducts. In the vicin-
ity of the urinary sinus the dorsal mesentery is rather thick and quite opaque, so that
it is difficult to determine whether collecting ducts are present. Nevertheless, two or
three collecting tubules were found entering the anterior end of each urinary sinus, as
shown for the right side in Text-figure 93.
The Anatomy of Chlamydoselachus 443
Transverse serial sections of the excretory system of specimen No. I were taken from
a region near the center of the body cavity, where the mesonephric ducts course in the
oviducal mesenteries; also from a region just posterior to the shell glands, where the ducts
run in the dorsal mesentery. In each case the right duct is decidedly smaller than the
left. In these sections of the mesenteries, the collecting tubules have much thicker walls
than the arteries and veins; so it is unlikely that, in dissections, any blood vessels were
mistaken for collecting tubules.
In specimen No. II, due to poor preservation and excessive mutilation of the mesen-
teries, only fragmentary portions of the mesonephric ducts and collecting tubules could
be found. In their size and distribution these portions conform to the general plan revealed
in my other specimens, particularly in No. I.
mes. d.
Text-figure 93.
Excretory organs of the right side of a female Chlamydoselachus in right lateral view, one-fourth
natural size. The broken line.indicates the junction of the dorsal mesentery with the oviducal _
mesenteries. The ventral region is uppermost.
c.t., collecting tubule; mes.d., mesonephric duct; ovd.mes., line of attachment of the right oviducal mesentery to the
right oviduct; 7.m., right mesonephros; r.u.s., right urinary sinus.
Drawn from specimen No. I in the American Museum of Natural History.
The posterior portions of the mesonephric ducts of Garman’s specimen (1885.2)
are illustrated in my Text-figure 92. In this figure, as already noted in my account of the
urinary sinuses, the mesonephric ducts are shown uniting to form a single large duct
posteriorly. Hawkes (1907) states that in the female Chlamydoselachus: “The same
mesentery which supports the oviduct also supports the urinary sinus and the mesone-
phric ducts. The latter pass from the kidney at regular distances, there being approxt
mately one to each myotome.”” This description of the mesonephric ducts is doubtless
intended for the collecting tubules.
In the account of the urethral apertures and urinary sinuses of my four specimens,
I have noted occasional deficiencies in these features on the right side. It remains to call
attention to some observed instances of deficiency in the duct system on the right side.
In specimen No. I the mesonephric ducts and collecting tubules, though well developed
on both sides, are slightly smaller on the right. In specimen No. III the right mesonephric
duct is of microscopic size, though the left duct is well developed for at least 50 mm.
in front of the urinary sinus. We might attribute these defects to pressure from the
right uterus, which is enormously enlarged while the young are being carried, were it
not for the fact that the most extensive defects occur in No. III, which is evidently not
quite mature. It seems more likely that the tendency to shift the burden of excretion on
to the left side is due to germinal variations which, however, are adaptive in view of the
unbalanced development of the reproductive organs of the right side.
444 Bashford Dean Memorial Volume
Among related forms, the female Heptanchus (Daniel, 1934) presents a much more
highly differentiated condition of the duct system. Only those collecting tubules from
a little more than the anterior halves of the mesonephroi drain into the mesonephric
ducts which, at the level of the ovaries, are coiled somewhat like the corresponding
portions in the male. This coiling is correlated with the presence of a rudimentary testis.
The remaining tubules, which lead from the broad and thick posterior portions of the
mesonephroi, open into a pair of very large tubular “ureters” which, in this region, lie
dorsal and lateral to the mesonephric ducts. Usually, each ureter joins a mesonephric
duct, posteriorly, before the combined vessels enter the single urinary sinus. In an
anomalous specimen with two urinary sinuses, right and left respectively, the meso-
nephric duct and the ureter of each side open separately into the urinary sinus.
The convergence and union of collecting tubules from the posterior portions of the
mesonephroi, to form “‘ureters” which enter the urinary sinus directly, are features
more characteristic of the highly differentiated elasmobranchs, especially the skates and
rays. Daniel (1934) states that the Wolffian duct (mesonephric duct) decreases in im-
portance as we approach the rays. In the female Squalus sucklii (Daniel, 1934, p. 295
and Fig. 253a) the condition is essentially the same as in Chlamydoselachus: the mesone-
phric duct receives the collecting tubules from practically the whole of the mesonephros.
This is probably the primitive condition. It seems extraordinary that Heptanchus, in
many respects one of the most primitive of living sharks, should have departed so far
from this archaic type of duct system.
GENITAL ORGANS OF THE FEMALE
From an inspection of Text-figures 85 to 88, it will be seen that my four specimens
display various degrees of development of the genital organs. Some of these differences
are certainly associated with age, others may possibly be concerned with a sexual cycle.
Though specimen No. IV is almost as large as the largest, its reproductive system retains
strict bilateral symmetry, and is obviously immature. In all the other specimens the
reproductive organs are better developed on the right side save that in No. III, which is
probably not quite mature, the left ovary shows a slightly more advanced stage of de-
velopment than the right. Specimens I and II are fully mature. Some structures seem
better developed in No. II than in No. I, but since it is probable that there is a definite
breeding season (Gudger and Smith, 1933, p. 302) these differences may be correlated
with a sexual cycle.
The largest known female, collected in Japan by Dr. Bashford Dean, had a total
length of 1960 mm. The average length for 35 females, comprising all known post-natal
female specimens for which the length has been recorded, is 1532 mm. (Gudger and Smith,
1933, Table V, p. 263). We do not know how many of these were sexually mature, but
only two of them had a length of less than 1220 mm. My two fully mature female
specimens, Nos. I and II, measure 1350 mm. and 1485 mm. respectively. My largest
specimen, No. III, has a total length of 1550 mm., yet it seems not quite mature. My
The Anatomy of Chlamydoselachus 445
quite immature specimen, No. IV, has a total length of 1398 mm. It is evident that,
allowing for individual variations, the female Chlamydoselachus reaches almost or quite
full size before attaining sexual maturity.
Tue Ovaries.—In Chlamydoselachus, the ovaries (Text-figures 85 to 88) are a pair
of elongate, more or less flattened organs situated in the anterior part of the body cavity
and attached, rather indirectly, to the dorsal body wall by means of broad mesenteries.
In specimens I and IJ, throughout their entire length the ovaries are attached by their
special mesenteries (mesovaria) to the ventrolateral surfaces of the oviducts including the
shell glands. In my immature specimen, No. IV, the ovarian mesenteries are attached
to the median dorsal mesentery just ventral to the attachments of the oviducts. In
No. III the ovarian mesenteries are attached as in No. IV, save that where these mesen-
teries pass along the ventral surfaces of the shell glands they are fused to the latter
organs. In Text-figures 85 to 88 the ovaries are displaced laterally as far as their attach
ments allow.
In specimen No. IV the two ovaries (Text-figure 85) are much alike. The length of
each ovary is about 180 mm., the maximum width (near the anterior end) is 20 mm., and
the maximum thickness is 6 mm. The largest follicles, which are in a collapsed and
flattened condition, measure only 10 mm. in their greater diameter. Since the mature egg
may be 100 mm. long and 60 mm. wide—measurements based on Nishikawa’s (1898) Fig.
1, pl. I[V—it is evident that, in the ovaries under consideration, the ovocytes are very
incompletely developed. There are no ruptured follicles indicating that ova have been
liberated. Only the largest follicles are represented on the ventral surface. The dorsal
surface shows, in addition to the large follicles, many smaller ones.
In specimen No. III the ovaries (Text-figure 86) are of almost equal size but the
left is slightly better developed. In each ovary, the largest follicles are situated along the
lateral margin. Since the largest follicle has a diameter of only 17 mm., it is evident that
the ovocytes are decidedly immature.
In specimen No. I the posterior part of the right ovary (Text-figure 87) is missing,
and has apparently been cut away. From the shape of the remaining portion, | infer that
this ovary was originally much larger than the left one which is intact. No follicles are
represented on the ventral surface of either ovary, but on the dorsal side of the left
ovary some small follicles, none more than 2 or 3 mm. in diameter, were found.
In specimen No. II the posterior part of the right ovary (Text-figure 88) is missing.
The preservation of this organ is very poor, so that it is difficult to distinguish a cut edge
from a mutilation produced by handling. Doubtless the rupture of large follicles has
played a part in the disintegration or contraction of this ovary. No follicles are recog-
nizable from the ventral surface. On the dorsal surface are protuberances due to the
presence of many small follicles, none exceeding 4 mm. in diameter; there is also a con-
cavity, 15 mm. in diameter, which represents the persisting half of a follicle. It is not
likely that this follicle has ruptured naturally. In the left ovary no follicles are recog-
446 Bashford Dean Memorial Volume
nizable from the ventral surface, and the largest follicles represented on the dorsal
surface measure only 6 mm. in diameter.
Garman’s (1885.2) figure, reproduced as my Text-figure 94, portrays the ovaries
of his specimen. He states that the ovaries had been badly preserved and that they were
much torn. Hawkes (1907) writes that the ovaries of Chlamydoselachus are diffuse
bodies attached by broad mesenteries to the line of attachment of the “‘stomach”’ mesen-
tery. The right ovary is placed somewhat more anteriorly than the left.
In Heptanchus (Daniel, 1934) and in Hexanchus (Semper, 1875, Fig. 1, pl. XIV),
a rudimentary testis is associated with each ovary. In Heptanchus maculatus this testis
lies in the mesovarium, at the base of the ovary, and runs parallel with the ovary. The
Text-figure 94.
Ovaries and oviducts of Chlamydoselachus, drawn one-half natural size.
ng, nidamental gland; 0, ovary.
Printed from the original wood-cut after the drawing by Paulus Roetter for Garman, 1885.2, Fig. 1, pl. XIX.
rudimentary testis consists of an anterior larger portion, and a marked swelling or ridge
which extends practically the entire length of the ovary.
Tue Ovipucts.—The oviducts of my four specimens are shown, in ventral view, in
Text-figures 85 to 88 inclusive. In specimen No. IV there is but slight differentiation in the
regions of the future uteri (ut.) and shell glands (s.g.); all parts of the oviducal system show
strict bilateral symmetry save that the rudiment of the right shell gland is slightly larger
than the rudiment of the left, and the right ventral ligament is quite noticeably larger than
the left. In specimen No. IH, all the oviducal organs of the right side are decidedly larger
than those of the left. The discrepancy is even greater in my specimens Iand II. To be
sure, in specimen No. I a large part of the uterus has been cut away, but the form of the
remaining portion gives evidence of the original size. I conclude that, so far as one can
judge from the specimens at hand, only the right oviduct is ordinarily functional, but the
degree of development attained by the left oviduct is such that it might possibly become
functional. In any case, the oviduct proper must become greatly distended while an egg
(60 x 100 mm.) is passing through it, and some idea of the size of the uterus after it has
contained developing embryos may be obtained from Text-figures 87 and 88.
The Anatomy of Chlamydoselachus 447
The common opening (ostium abdominale tubae uterinae) from the body cavity into
the oviducts is situated in the region of junction of the oviducts at the extreme anterior
end of the body cavity, ventral to the root of the liver. In specimen No. II (Text-figure 88)
this opening is almost divided into two, one for each oviduct, which face somewhat medial-
ly. It seems almost incredible that so large an egg as that of Chlamydoselachus can find
its way into one of these openings, though the fluted, funnel-shaped ostium is evidently
capable of distention.
Throughout almost their entire lengths the oviducts are supported by special mesen-
teries attached to the median dorsal mesentery. The only exceptions are found anteriorly,
where in front of the shell glands the oviducts diverge to course along the dorsal, lateral
and ventral walls of the body cavity, and then unite ventral to the root of the liver. In
specimen No. IV each oviduct, where it traverses the lateral wall of the body cavity, is
attached to this wall by a narrow mesentery. This mesentery, which we may call the
dorsolateral mesentery of the oviduct, is not shown in Text-figure 85. It is not present
in my older specimens where the corresponding part of the oviduct is closely applied to
the body wall and is merely covered by the peritoneum. In all my specimens, special
provision is made for the support of the ventral portions of the oviducts. In specimens
IV and III this support is furnished by a pair of ventral ligaments (Text-figures 85 and 86),
which are strong special mesenteries. Each has one end fastened to the ventrolateral
portion of the oviduct and the other end attached to the ventral body wall near the midline.
In my older specimens, Nos. I and II, these ligaments (Text-figures 87 and 88) are shorter
and broader; they differ, too, in their histological structure, since they blend with the
substance of the oviducts.
In its enlarged state, on the right sides of my adult specimens, the so-called uterus has
thin walls, a velvety inner surface and a fairly rich blood supply. The mucous membrane
is not sufficiently well preserved to permit a study of the finer structure.
The anterior portions of the oviducts (“some twelve inches in length”) of Garman’s
specimen (1885.2) are represented in my Text-figure 94. It is interesting to note that there
are two ostia, entirely separate from one another (compare my Text-figures 85 to 88 inclu-
sive). Of his specimen Garman says: “Three inches from the anterior end of one of the
oviducts it bore a nidamental gland; the gland of the other tube was an inch farther back.
A piece left at the cloaca showed one of the ducts greatly distended, possibly with young
that had hatched within it. Only one of the tubes had been in use.” In Text-figure 92
the opening of the oviduct that had not been expanded is shown on the left side, the
other (right side) having been cut open to show the internal arrangement. Garman’s
intricate description, illustrated by his Fig. C, pl. XX, of the internal structure of the
nidamental gland (shell gland) is too involved for consideration here. It should be com-
pared with Borcéa’s account (1905, pp. 419-427, Text-figs. 93, 94 and 95) of the structure
of the nidamental gland of Scyllium.
Collett’s (1897) puzzling description of the oviducts and “uteri” of his large female
448 Bashford Dean Memorial Volume
specimen is quoted here with the comment that nowhere in his paper do I find any
mention of the ovaries:
The oviducts were extremely long, both being of about equal length. Towards their
upper ends [sic] each expands to a uterus-like sack, of which the right is somewhat larger
than the left; both contained immature eggs. Below this expansion the oviducts are quite
narrow, but subsequently expand slightly downwards towards the abdominal pores. The
total length of each oviduct is about 900 mm.
The right “uterus” was 240 mm. in length, and contained 10 large eggs, about the size
of the yolk of a small hen’s egg, but some varied in size. There were, besides, about 30 lesser
yolks of the size of large and small peas, as well as a few bigger ones about the size of
the yolk of a pigeon’s egg. The length of the left uterus was 220 mm., and it contained 5
large yolks, and about 20 small ones.
Nishikawa (1898) states that the left oviduct of Chlamydoselachus is always rudi-
mentary, and the nidamental gland of the right side is better developed than that of the
opposite side. The right oviduct is much distended when it contains from 3 to 12 eggs,
these numbers being the limits observed in 7 specimens. Each egg is 110 to 120 mm. long
(transverse diameter not stated), while the oviduct is only 600 mm. long. As already
stated, measurements based on Nishikawa’s Fig. 1, pl. IV, representing an egg within its
envelopes, give a length of 100 mm. and a transverse diameter of 60 mm. Doubtless
changes in the form of the egg occur, since it must be compressed while passing through
the oviduct proper. In a footnote to Nishikawa’s paper, S. Goto, who prepared the
manuscript for publication, states that when no eggs are contained there is no perceptible
difference in size between the two oviducts. In another foot-note Goto writes: “Mr.
Nishikawa tells me . . . that the female genital organs of Chlamydoselachus are essentially
like those of other sharks, and I can confirm his statement from a passing examination of
a specimen brought some time ago to my laboratory. Collett’s description of these organs
appears to me irrelevant.”
Hawkes’ (1907, pp. 475-476) description of the oviducts of the female Chlamydo-
selachus is so instructive that it is quoted entire:
The oviducts have large funnels which open ventrad to the stomach, instead of dorsad
as is usually the case. The edges of the funnels are irregular and spreading, and are united
in the median ventral line to one another, thus forming one large funnel. The anterior edges
of the funnels become united to the anterior wall of the body cavity, whilst the posterior
edges of the united fimbriae hang free. A triangular dorsal pouch is thus made between the
wall of the abdominal cavity and the funnel. As this pouch is in the usual position of
the coelomic openings of the oviduct, the eggs would tend to pass into it instead of into the
latter, if this were not prevented by the unusual position of the ovaries which are ventral to
the oviducts. For the first 6 cm. the oviduct is a straight tube, the walls of which are lined
with numerous laminae. This region passes into the oviducal gland, the walls of which are
much thickened, except along two longitudinal lines which are approximately dorsal and
ventral. The length of the gland is 3 cm. Its interior is covered by fine laminae continuous
with those in the preceding and succeeding portions of the oviduct. The laminae run spirally,
and are very close together, instead of longitudinally and somewhat separated, as is the case
throughout the remainder of the oviduct. The transverse deeper groove in the oviducal
The Anatomy of Chlamydoselachus 449
gland mentioned by Garman ]1885.2] was found in the specimen examined. Passing from
the oviducal glands, the oviducts regain their original diameter, but the walls are smoother,
the laminae being reduced to slight striae. When the oviduct reaches the level of the anterior
end of the colon, it enlarges. The enlargement is gradual and only increased in diameter about
fourfold on the left side, but on the right the enlargement is sudden and very apparent, the
diameter increasing 14 to 15 times. This region in addition to being enlarged has folded
walls, in which occur one large and several small areas of dilated blood-vessels. The largest
blood plexus occupies about one-third of the right side of the oviduct. In connection with
each plexus, on its dorsal side, the oviducal wall is thickened over an area which equals the
plexus in length and breadth. The enlarged vessels apparently supplied these thickened
areas. The condition of the oviduct thus described suggests that this portion of the oviduct
acts as a functional uterus, and that therefore Chlamydoselachus produces the young alive, as
suggested by Garman. The final portion of the oviduct, which succeeds the uterine, has
smooth walls and a large diameter, the latter gradually diminishing towards the cloaca.
This region divides the functional uterus from the cloaca, thus functionally representing the
the vagina of higher types. The opening of the right enlarged oviduct [Text-figure 90a, R.Ov. |
has acquired a median position, the left oviducal opening [ L.Ov. | lying cephalad to it.
Deinega’s (1925) small half-tone figure of the abdominal viscera of a female Chlamy-
doselachus is printed on unsuitable paper, so that details are obscure. It is chiefly remark-
able in that it shows a complete right uterus which is even larger than that of my specimen
No. IJ. Its length, including the part bulging anteriorly, is equal to about five-sevenths
of the length of the body cavity. It is somewhat kidney-shaped, with a maximum width
of more than one-fourth its length. The left oviduct is not conspicuously enlarged in its
uterine portion.
Hawkes’s observations on the presence of vascular plexuses in thickened portions
of the uterine wall suggest a physiological relation between the maternal tissues and the
young. I do not know whether the young are carried after the exhaustion of their store
of yolk. It seems likely, however, that the young sharks are born as soon as, or even
before, the yolk is entirely utilized. The largest known intra-uterine specimen, taken by Dr.
Bashford Dean, was a well-formed shark, 390 mm. (15.35 in.) long, yet its yolk sac meas-
ured 100 x70 mm. Additional data are given by Gudger and Smith (1933, pp. 298-301).
It is unnecessary to review the evidence that the genital organs of the right side
alone are functional in the female Chlamydoselachus. There is not a single known instance
of complete development of the reproductive organs of the left side. Yet it must be borne
in mind that the number of specimens that have been described is still very small. The
organs of the left side are developed to such a degree that they can scarcely be called
rudimentary. In view of the great variability found in many other organs of Chlamy-
doselachus, one should not be surprised if the examination of additional material should
reveal cases in which the genital organs of the left side, or of both sides, are functional.
In the adult female Heptanchus as described by Daniel (1934), the general plan of the
oviducts is much the same as in the immature female Chlamydoselachus. According to
Daniel “the oviduct . . . is not so greatly enlarged in Heptanchus as in many other Elasmo-
branchs in which it forms the conspicuous uterus.” In the absence of any definite state-
450 Bashford Dean Memorial Volume
ment to the contrary, one might assume that the two oviducts of Heptanchus are of
equal size; but if I interpret Daniel’s fig. 251a correctly, the right oviduct is considerably
larger than the left.
UROGENITAL SYSTEM OF THE MALE
I have no adult male specimens of Chlamydoselachus, and the literature on the male
reproductive organs is very fragmentary. No description of the mesonephroi in the
male has been found. It seems best to present the observations of each author in chrono-
logical order, reserving for special treatment the myxopterygia or “‘claspers.”
EXCRETORY AND INTERNAL GENITAL ORGANS
Giunther’s (1887) material consisted of two males, the larger 1473 mm. long. Both
specimens seemed to be sexually mature. The testes are narrow elongate bodies of
nearly equal size, about 127 mm. long and 13 mm. broad at the broadest part. They
reach close to the anterior end of the abdominal cavity. In one of the males the arrange-
ment of the urogenital organs and ducts, as well as of the external openings, is perfectly
symmetrical (Figure 17, plate V), while in the other (Figures 18 and 19, plate V) the
left side shows a much more highly developed condition than the right. In the former
(bilaterally symmetrical) specimen, the urogenital organs are not further described. In
the latter specimen the left ductus deferens is much wider than the right, and its interior
contains low, circular, close-set septa (Figure 16, plate IV). Only faint traces of septa
can be seen in the right duct. They are limited to the lower three or four inches of the
duct. The left ductus deferens opens into “the urinary bladder, if a bottle-shaped
dilatation which terminates externally in a single small conical papilla may be so called.”
The right ductus deferens opens by a slit at the side of the papilla directly into the cloaca.
It is not clear how many male specimens Hawkes (1907) examined. In describing
the urogenital system of the male, she refers to “my specimen,” but in her description of
the abdominal pores she writes concerning “one of the males examined.” She states
that in the male there are two urogenital apertures (Text-figure 90s, after Hawkes),
each being the outlet of an oval urogenital sinus (BI.) which Gunther described as a urinary
bladder. Anteriorly, the sinus communicates by a very small aperture with a second and
larger chamber (R.S.), which is continuous with the ductus deferens (V.D.) or meso-
nephric duct, and possibly functions as a seminal vesicle. The ductus deferens has
(presumably on its inner surface) one or more projecting spiral folds which run from one
end of the duct to the other. In the posterior 100 mm. of the length of the duct, the
folds are very obvious, but from this point forward they become almost invisible to the
naked eye. In the posterior part of the duct the folds are very close together (Gunther
describes them as “circular” folds). Hawkes further states that the lumen of the left
ductus deferens (which Gunther found, in one of his specimens, to be better developed
than the right) is very irregular in diameter “in my specimen.” At its widest, the duct
measures about 5 mm., but where narrowest it allows only the passage of a bristle.
Since the excretory and the internal genital organs of the male Chlamydoselachus
are so imperfectly known, a comparison with other elasmobranchs would be unprofitable.
The Anatomy of Chlamydoselachus 451
MYXOPTERYGIA OR CLASPERS
The superficial appearance of the intromittent organs or so-called claspers of the male
Chlamydoselachus is illustrated in Figure 20, plate V, after Gunther; Text-figures 95 to
97, after LeighSharpe. The skeletal anatomy has been discussed in the section on the
endoskeleton, and is illustrated by Text-figure 46, p. 375, after Braus; Text-figure 47, p.
377, after Giinther; Figure 21, plate V, after Goodey; and Text-figure 1154 (p. 472),
after LeighSharpe. The muscles of the claspers have been considered in the section on
the muscular system, and are illustrated by Figures 22 and 23, plate V, after Goodey;
also by Text-figure 1158 (p. 472), after Leigh Sharpe. The peculiar blood vessels of the
claspers are described in the section on the blood-vascular system. The present account
deals with the general form and structure of the claspers, together with some inferences
as to the manner in which they function.
As an introduction to the study of the claspers I can do no better than to quote the
following from LeighSharpe (1920, pp. 245-246):
Text-figure 96.
Ventral view of the pelvic region of a male
Chlamydoselachus with claspers anteroflexed as
in copula: A, with the clasper groove closed;
B, with the clasper groove forced open.
Text-figure 95.
Ventral view of the pelvic region of
a male Chlamydoselachus, showing myx-
opterygia or claspers.
Cav., projection of cavity. A le C ae
Nive \ustinsirrass, WGH4, TD ih, wy AOS p., apopyle; Cav., cavity; Cl.Gr., clasper groove; H.,
hypopyle.
After Leigh-Sharpe, 1926, Fig. 2, p. 309.
452 Bashford Dean Memorial Volume
In the male elasmobranchs, where fertilization is internal, the basal element of each pelvic
fin (basipterygium) is prolonged to form a stout backwardly directed skeletal rod supporting
a portion of the fin which is demarcated from the remainder and especially modified to
form a copulatory organ, the clasper.
The clasper is rolled up in a manner resembling a scroll, so that instead of being a groove,
as it is usually described, it is a sufficiently closed tube along the greater portion of its length,
though the edges may not be and usually are not completely fused but overlapping. This
tube is one along which spermatozoa pass, in-
jected by an apparatus, the siphon, which has
not hitherto been sufficiently well known and
investigated.
The anterior proximal opening into this
scroll-like clasper groove or tube will be hereafter
known as the apopyle, the posterior, distal exit
from the same as the hypopyle. In the sharks
and dogfish the apopyle is close to the cloacal
aperture, while in the skates it is some consid-
erable distance posterior to it, an inch or more
in a moderately sized adult.
Leading into the apopyle by a narrow ap-
erture, so as to communicate with the clasper
tube on either side, is a large cavity, the siphon,
a sac with extremely muscular walls, situated
immediately below the corium of the ventral sur-
face of the abdomen, frequently several inches
in length, close to the median line, and ending
blindly, having no communication with the
coelom, and whose function and significance it
will be my endeavor to elucidate.
In the skates, on the other hand, no such
hollow sac is found, but its place is taken by the
clasper gland, contained in a sac which it com-
pletely fills. This gland has long been recognized,
but its containing sac does not appear up to the
present to have been demonstrated to be ho-
Cav., cavity; Cl.Gr., clasper groove; I.V., iliac vein; U-P., mologous with eas CRE SipROR GI Une alban
urogenital papilla; V.F., ventral fin; V.S., venous sinus. and dogfish, which is but little known.
After Leigh-Sharpe, 1926, Fig. 4, p. 311. Other accessory structures may be present
on the claspers, such as the spurs and the like
in Acanthias, but of these none attains such importance and is more frequently present
than a fan-like expansion at the distal end of the clasper, the rhipidion, whose function is to
spray the spermatozoa in all directions ina radiating manner. . .. The rhipidion attains a greater
development in the skates than in the sharks.
Zé,
Text-figure 97.
Pelvic fin region of a male Chlamydoselachus:
A, ventral aspect; B, left lateral aspect.
The manner in which the various parts of a myxopterygium, particularly the siphon,
function is described at length by LeighSharpe (1920, pp. 247-251) in the case of
Scyllium catulus.
The Anatomy of Chlamydoselachus 453
Concerning the external anatomy of the myxopterygium of Chlamydoselachus,
Goodey (1910.1, p. 564) states that:
On the dorsal side of each appendage, bounded by muscles, is the channel, which,
toward its posterior end, becomes somewhat lateral in position and is bounded here by the
knife-edged, movable terminal cartilages T.d. and T.v. [my Figure 22, plate V]. Ina ventral
aspect [my Figure 23, plate V] the most prominent feature of the appendage is the glandular
sac [S] and compressor muscle, covered with loosely fitting, soft skin. The skin covering
the sac and the termina Iparts of the appendages is very soft and is entirely free from
dermal spines.
For a more comprehensive description of the claspers of Chlamydoselachus, we are
indebted to Leigh-Sharpe (1926) whose account is illustrated by my Text-figures 95 to 97,
and 115 (p. 472). From LeighSharpe (pp. 308-311) I quote as follows:
This genus [Chlamydoselachus], though included from other characters in the Proto-
selachii, does not show any afhnities with Notidanus in its copulatory organs. The claspers,
far from being primitive, are long, tapering, and somewhat slender, though possessing strong
skeletal supports, 13 cm. in length in this specimen, and devoid of dermal denticles (Fig. 1)
[my Text-figure 95]. The clasper groove is long and closed for the greater part of its length
(Fig. 2) [my Text-figure 96a], and the apopyle is small. The apex of the clasper is capable
of expansion or erection, like a bivalve shell, the larger valve acting as a cover rhipidion. -
The true rhipidion may be represented by a small protuberance, not far from the apex, which
contains a separate cartilage, and is discernible in figure 5 [my Text-figure 115a, p. 472]. On
this occasion the animal’s left clasper has been dissected instead of the right as heretofore.
There is no siphon present, but situate on the inner ventral aspect of the proximal end of
the clasper is a large cavity which opens dorsally by the clasper groove of which it forms an
expansion. In these two characters a startling similarity is shown to the Holocephali, more
expecially to Rhinochimaera, and, as I was unable to dissect the latter, the details of the
present type are portrayed more fully.
The cavity, which occupies roughly three-quarters of the length of the clasper parallel
with the clasper groove, is much distended, with powerful muscular walls, supported by
two radial cartilages outspread in a fan-wise manner (Figs. 4 and 5a) [my Text-figures 97
and 115a]. I have no doubt that it can be used for pumping spermatozoa, being, therefore,
analogous with a siphon; and in this it agrees with the cavity of Callorhynchus and Rhino-
chimaera, though not with that of Cestracion (which possesses a siphon) and some species of
Chimaera. When the claspers are anteroflexed as in copula (Fig. 2) [my Text-figure 96], the
cavity collapses and is compressed. By a comparison of measurements, it seems certain that
the posterior part of the cavity must be included in that part of the clasper which is introduced
into the oviduct of the female.
The simplicity of the clasper has prompted a more detailed account of its anatomy.
Regan (1906.2, p. 740) states that the myxopterygium of Chlamydoselachus and the
notidanids is a more primitive structure than that of the galeoid sharks.
THE ABDOMINAL PORES
Although there is no immediate evidence that the abdominal pores have anything
to do with the urogenital system, it is convenient to consider them here, since they are
situated near the urogenital sinus and are often figured with it.
454 Bashford Dean Memorial Volume
The abdominal pores of my female specimens of Chlamydoselachus are a pair of
short canals leading from the ventral portion of the body cavity, by the most direct
route, to their external openings on each side of the ventral surface of the body just
posterior to the cloaca. The body cavity extends along each side of the cloaca, but not
so far caudad in its ventral as in its dorsal portion. The difference (about 15 mm.) is
approximately equal to the length of the abdominal pores. The distal or superficial half
of each canal lies just beneath the integument which is usually upraised to form a low
ridge. The inner opening is somewhat funnel-shaped and is large enough to admit a pencil.
The canals, when probed from the body cavity, are found to be quite uniform in caliber,
well-rounded and about 5 mm. in diameter. The external openings (ab.p. in Text-figures
85 to 88) vary considerably in size. When well developed, as in specimens IV and III
(Text-figures 85 and 86) they are elliptical, about 8 mm. long, and face obliquely ventrad,
laterad and caudad. In specimens I and II (Text-figures 87 and 88) they are usually
Text-figure 98.
Pelvic fins, abdominal pores and
cloacal aperture of a 1220-mm.
female Chlamydoselachus.
After Garman, 1885.2, Pl. I.
round and comparatively small, but one is absent. On the right side of No. II the external
opening is so small that it barely admits a probe. In the single case (specimen No. J)
where an external opening is absent, the canal is fully developed internally but is closed
externally by the integument.
The external openings of the abdominal pores in Garman’s (1885.2) specimen, a large
female, are shown in his plates, reproduced as my Text-figures 98 and 89. Garman states
that the mouth of each abdominal pore is inflated into a broad flap, by which the pores
are hidden. Hawkes (1907), in a figure reproduced as my Text-figure 90a, shows the
cloacal region of a female with two closed abdominal pores.
The specimens thus far considered are all females. It remains to describe the condi-
tion of the abdominal pores in the male. Gunther’s (1887) illustrations include two
figures (my Figures 17 and 18, plate V) showing the abdominal pores of his male speci-
mens. One is normal, showing two open pores similar to those of the typical female;
the other is anomalous, possessing only a single abdominal pore, which is unusually large.
In his text, Giinther states that this single abdominal pore is situated immediately behind
the cloaca and ‘‘in the median line (or very slightly to the left of it)” but his figure shows
it definitely on the left side. Hawkes (1907) writes: “One of the males examined has
two abdominal pores of which the right is the better developed.” In the explanation of
her diagrammatic text-figure (my Text-figure 90s) the left pore is said to be closed.
From the meager evidence at hand it does not appear that there is any important
difference between the abdominal pores of the male and the female, but it is clear that
The Anatomy of Chlamydoselachus 455
both are decidedly variable. That they are not essential for the life of the fish is indicated
by Hawkes’ observation of an adult female with both abdominal pores closed.
PERICARDIO-PERITONEAL CANALS
In the embryonic development of higher vertebrates, the primitive coelomic cavity
becomes divided into three cavities, pericardial, pleural and peritoneal respectively. In
the adult elasmobranch there are only two coelomic cavities, pericardial and peritoneal,
and their separation is not quite complete. A pair of slender thin-walled canals, joined
Text-figure 99.
Diagrams showing the pericardio-peritoneal canals (dorsal views) in: A, an
adult Squalus; and B, an adult Scyllium. Dorsal parts removed by a hort
zontal cut. The canals below the esophagus are represented by dotted lines.
dcv, ductus Cuvieri; dm, dorsal mesentery; lig, lateral suspensory ligament of I, the liver; lo,ro,
left and right openings of the pericardio-peritoneal canals; oe, esophagus; p, pericardial coelom;
po, median opening of the pericardio-peritoneal canal into the pericardial coelom; rlig, right
lateral suspensory fold; sm, sub-esophageal lesser mesentery (hepato-enteric mesentery).
After Goodrich, 1918.1, Fig. 18.
at their pericardial ends to form a single large canal opening into the pericardial cavity
(Text-fig. 99), course posteriorly along the ventral wall of the esophagus to open by wide
apertures, thus placing the pericardial cavity in communication with the peritoneal
cavity—as in Squalus and Scylliwm (Goodrich, 1918.1, Fig. 18); and Raja (Monro, 1785).
Pericardio-peritoneal canals of selachians were first described and figured by Monro
in the skate. Balfour (1876-78) interpreted these canals as developmental arrests, but
Hochstetter (1900) claimed that in Acanthias the early communication between the
pericardial and peritoneal cavities became completely closed, and that the canal opening
from one to the other in the adult is a new formation. Goodrich (1918.1) investigated
the development of these canals not only in Squalus (Acanthias) but also in Scyllium,
concluding that Hochstetter was mistaken in his interpretation and that Balfour’s
view is essentially correct.
In each of my four large specimens of Chlamydoselachus, pericardio-peritoneal
canals were found. Since there is considerable variation in the structure and relations
of these canals, each specimen will be described separately.
456 Bashford Dean Memorial Volume
In specimen No. II the condition of the canals (Text-figure 100A) is most like that
described for other elasmobranchs, though some differences are obvious. On the anterior
surface of the posterior pericardium (p.p), close to its dorsal border, there is a large opening
(c.) leading into a shallow cavity. The width of the cavity (and of its opening) is about
12 mm.; its depth is only about 3 mm. This cavity, which I shall call the pericardio-
peritoneal sac, represents the fused portion of the two canals (7.p.c. and I. p.c.), which
open into it by apertures about 4 mm. in diameter. The canals were probed. Each is
about 4 mm. wide when collapsed, and is about 20 mm. long; the walls are very thin.
Text-figure 100.
Pericardio-peritoneal canals of Chlamydoselachus, leading from the pericardial
cavity (above) to the peritoneal cavity (below); ventral views, natural size.
c., common opening of the canals into the peritoneal cavity; d.p., dorsal pericardium; I.p.c., left
pericardio-peritoneal canal; es., esophagus; p.p., posterior pericardium; p.p.s., pericardio-peritoneal
sac formed by the fusion of right and left canals; r.p.c., right pericardio-peritoneal canal.
A is drawn from specimen No. II in the collection of the American Museum of Natural History;
B, from a specimen (No. IV) lent by Dr. E. Grace White.
The canals pass dorsad along the posterior surface of the pericardial wall to reach the
esophagus (es.), then caudad along the ventral surface of the esophagus, dorsal to the
liver, to open by wide crescentic apertures into the peritoneal cavity (Text-figure 100a).
In my specimen No. I, conditions are practically the same as in No. II save that the
pericardio-peritoneal sac is about 6 mm. wider than its opening into the pericardial
cavity, and that the right pericardio-peritoneal canal is closed at its posterior end.
In specimen No. III the common aperture and the pericardio-peritoneal sac are
much the same as in specimen No. IJ, but their situation on the posterior wall of the
pericardial cavity is a little further ventrad—not so close to the dorsal border as in the
preceding specimens. Thus the paired canals must pass a little further dorsad in order to
reach the esophagus. The canal on the right side is only 5 mm. long and does not reach
the esophagus. The canal on the left side is 10 mm. long and turns posteriorly upon
reaching the esophagus. Both canals are closed at their posterior ends.
The Anatomy of Chlamydoselachus 457
In specimen No. IV (Text-figure 100s) the common aperture (c.) of the pericardio-
peritoneal canal is situated as in No. III, a few millimeters from the dorsal border of the
posterior pericardial wall. This opening has about the same size (12 mm. wide) as the
corresponding openings in the other specimens; but it is bordered laterally by thin lips
due to an extension of the pericardio-peritoneal sac (p. p. s.) which is about 22 mm. wide
though no deeper than in the other specimens. The openings into the paired canals
are smaller, and the canals are more slender. Each canal is about 13 mm. long and ends
in contact with the esophagus at the extreme anterior end of the peritoneal cavity. Both
canals end blindly.
In two respects the pericardio-peritoneal canals of Chlamydoselachus differ from the
condition typical for elasmobranchs: the anterior unpaired portion is extremely short
and broad, forming a shallow sac; and the paired canals often end blindly. Of the eight
canals in my four specimens, five are closed at their posterior ends. It is noteworthy
that the closed canals are usually smaller than the open ones. It is apparent that there
is a tendency toward obliteration of the canals, and this may be interpreted as a depar-
ture from primitive conditions.
BLOOD-V ASCULAR SYSTEM
Studies of the blood-vascular system of Chlamydoselachus have been almost entirely
limited to (1) the heart; (2) the arteries anterior to the heart; (3) the large venous trunks;
and (4) the venous sinuses of the claspers. These comprise, however, the most interesting
and complex portions of this system. In my own material, only a few portions of the
blood-vascular system are in a condition favorable for investigation. I have therefore
studied only the heart and the blood vessels of the gills.
THE HEART
Since there is much variation in the names that have been applied, by different
authors, to the anterior division of the elasmobranch heart, it is desirable to justify my
choice of the term conus arteriosus, which is used throughout this section. The present
status of our knowledge of the homologies of this portion of the heart is set forth by
Goodrich (1930, p. 538) in the following words:
There has been considerable confusion in the nomenclature of the anterior region of the
heart. Bulbus cordis is the name now generally applied by embryologists to the anterior
chamber. But the name conus arteriosus, introduced by Gegenbaur to designate the anterior
muscular region of the Selachian heart, is often given to it. Moreover, the Selachian conus
does not [precisely?] correspond to that part of the heart so called in human anatomy. It
is best, then, to apply the name bulbus cordis, introduced by A. Langer, to the embryonic
structure throughout the Craniata, and keep the name conus arteriosus for the adult muscular
contractile chamber derived from it in Pisces and Amphibia.
Garman’s figures of the heart of Chlamydoselachus are reproduced as my Text-figures
1014 and 101s. Of his specimen Garman (1885.2, pp. 18 and 19) writes:
458
Bashford Dean Memorial Volume
Departing considerably from the conventional form of heart, this genus presents a shape
that is somewhat peculiar. Seen from below, it has a small subquadrangular ventricle,
a large auricle, and a long bulbus arteriosus. The ventricle measures nearly three-quarters
of an inch in either width or length. When filled, the auricle is subtriangular, and measures
on each side an inch and a half. The bulbus is almost twice as long as the ventricle. Behind
the auricle,and above and behind the ventricle, lies the sinus, which has a capacity that nearly
Text-figure 101.
Heart of Chlamydoselachus: A, in ventral view; B, longitudinal section showing cavity
in ventricle, also valves of the bulbus (conus) arteriosus.
1, auricle (atrium); 2, ventricle; 3, bulbus (conus) arteriosus; 4, sinus venosus; 5, dark tissue between cardiac
and abdominal chambers; 6, cavity in ventricle; 7, valves in bulbus (conus).
Printed from original wood-cuts after drawings by Paulus Roetter for Garman, 1885.2, Pls. XVII and XVIII.
equals the bulk of the ventricle. From it the opening into the auricle is guarded by a pair of
valves that are without chordae. The auriculo-ventricular opening is furnished with a pair of
valves provided with chordae tendineae. In the ventricle the cavity or chamber is small; its
outlines in longitudinal section resemble those of a pipe with a short stem, the stem being
directed toward the left upper side and the bowl toward the bulbus. Along the inside of
the passage (Fig. B, pl. XVIII) [my Text-figure 1018], the muscles lie in bands (columnae)
The Anatomy of Chlamydoselachus 459
loosely laid one upon another, those in the posterior section, or stem of the pipe, running
transversely, and those of the anterior section being longitudinal.
Behind the ventricle, in the partition, between the peritoneum and the pericardium, there
is a spongy mass of dark tissue an eighth of an inch in thickness.
Gunther (1887) had available for examination three well-preserved specimens of
Chlamydoselachus. His drawings, illustrating the external form of the heart and the
configuration of the valves of the conus, are reproduced as my Text-figures 102 and 102s.
Gunther gives no general description of the heart, but it will be noticed that his figure
confirms Garman’s (1885.2) statement con-
cerning its form.
Ayers’ (1889) Fig. 2 (reproduced as my
Text-figure 105, p. 462) portrays the heart of
Chlamydoselachus in sectional view, and the
drawing appears to be semi-diagrammatic.
Therefore this figure does not give us much
information concerning the form of the heart
in his specimen. His description (p. 194) of
the conus arteriosus follows:
The conus arteriosus forms a thick
spindle-shaped trunk about an inch long and
one-fourth of an inch in diameter. It is pro-
vided with six rows of valves, all of which
are quite small, except the anterior set of
three, which are large, tridentate, and
formed of a white tough tissue of a cartilag-
inous consistency.
Text-figure 102.
Heart of Chlamydoselachus: A, in ventral view; B,
conus arteriosus opened longitudinally to show the
arrangement of the valves.
7, right atrium; I, left atrium.
After Giinther, 1887, Figs. 7 and 8, pl. LXV.
My observations do not entirely agree with those of Garman and Gunther regarding
the proportions of certain parts of the heart. In my three specimens (from the fourth
specimen the heart had been removed) the conus arteriosus is indeed long, as in Garman’s,
Gunther’s, and Ayers’ specimens; but the ventricle, even when empty, is larger than it
appears in the figures by Garman and Gunther, and the size of the atrium is variable.
Text-figure 103 is drawn from my specimen No. III in which the ventricle (v.) is moder-
ately distended with blood. The atrium (atr.) is empty, but in its flattened condition
it retains a smoothly rounded outline, as shown in the figure. The size of the atrium is
somewhat exaggerated due to its flattened condition; nevertheless, the atrium of this
Text-figure 103.
Hearts of two specimens of Chlamydosel-
achus, in ventral view, one-half natural size:
A, drawn from No. III; B, from No. II.
atr., atrium; c.c.v., common cardinal vein; co., conus
arteriosus; s.v., sinus venosus; v., ventricle.
Drawn from specimens in the American Museum.
< De
460 Bashford Dean Memorial Volume
specimen is certainly large. In specimen No. II (Text-figure 103B) the ventricle (v.) is
partially distended with blood. Its size equals that of No. II but its form is quite different,
more nearly resembling that of the human ventricles. The conus (co.) is so long that
proximal and distal halves, when at rest, are bent almost at right angles to each other
in order to find room within the pericardial cavity. In specimen No. | the proportions
are much the same as in No. III, but the ventricle, which is empty, is kidney-shaped
with its long axis extending transversely and its lesser curvature facing anteriorly. In
the undisturbed condition, the left half of the ventricle was folded dorsal to the right
half. In this condition, when viewed from the ventral aspect, the ventricle of No. I
has much the same appearance as in Gunther’s figure. Thus in my three specimens, even
after allowing for differences due to expansion and contraction of its chambers, the form
of the heart as viewed from the ventral aspect varies considerably, but the ventricles
are uniformly larger than those shown in Garman’s and Gunther’s figures.
In my three specimens, the sinus venosus (s.v. in Text-figure 1034) and the common
cardinal veins or ducts of Cuvier (c.c.) are of the usual elasmobranch type, but seem rather
large. Of the mass of spongy tissue in the posterior pericardial wall, mentioned by
Garman, I can find no trace.
Concerning the valves of the conus (bulbus) arteriosus in the specimen illus-
trated by my Text-figure 101s, Garman (1885.2, p. 18) writes: ““The bulbus contains
six rows of valves, or seven if we count the single valve nearest the ventricle as a row.
Two or three of the posterior series have chordae tendineae.” Gunther’s (1887, p. 4)
description of the conus arteriosus in his specimen follows:
The conus arteriosus (Figs. 7 and 8) [my Text-figure 102] is of considerable length,
slightly bent towards the right, and of nearly the same diameter throughout. No special valve
separates it from the ventricle. I find the valves much more regularly arranged than would
appear from the figure given by Garman. They form three longitudinal and six transverse
rows (Fig. 8). The largest are those of the distal transverse row, placed close to the end of the
conus, and somewhat more distant from the next row than the five other rows are from each
other. The next largest valves are those of the proximal row, those of the second and third
being smaller, and those of the fourth still smaller, with only partially free anterior margins;
the valves of the fifth row are quite rudimentary, and two of them merely indicated as raised
papillae, which are confluent with those of the fourth row. Finally, a fourth intermediate
longitudinal series is indicated by two minute valves, belonging to the first and second
transverse rows. The larger valves are provided with tendinous chordae.
The valves of the conus in my three specimens are regularly arranged in transverse
rows, but the arrangement in longitudinal rows is not always perfect. In specimen No.
III the valves are the largest, but this may be due to the fact that they are best preserved.
In this specimen there are five transverse rows, with a space of double the usual extent
between the fourth and fifth rows counting from the proximal end of the conus. The
valves of the distal row are much the largest, as in Garman’s specimen; the valves of the
two proximal rows rank next in size. The numbers of valves in each row, reckoning from
the proximal end of the conus, are 3, 4, 4, 5, and 3 respectively. In specimen No. II there
The Anatomy of Chlamydoselachus 461
are four transverse rows with at least three valves in each row—the precise number is
uncertain. The same may be said of No. I.
As stated by Garman (1885.2), generally among sharks the conus is shorter and the
transverse rows of valves less numerous, than in Chlamydoselachus. In Garman’s Pls.
56 and 57 (1913) we find illustrated (without text) the external form of the heart, and
the form and arrangement of the valves of the conus arteriosus, in many different species
of elasmobranchs. The heart of Heptanchus maculatus (Text-figure 1044) has a fairly
long conus arteriosus—longer than that of Hep-
tranchias (Heptanchus) perlo (Garman, 1913, Fig.
1, pl. 56) but shorter than that of Chlamy-
doselachus. In Heptanchus (Text-figure 1048)
the valves of the conus arteriosus show partial
suppression of the second row counting from the
distal end of the conus, and complete suppression
of the third row.
THE BLOOD VESSELS
For descriptions of the blood vessels of
Chlamydoselachus, we must rely almost entirely
on the work of Ayers (1889) and Allis (1908, 1911,
1912 and 1923). In several respects, the condition
of the arteries as described and portrayed by
Ayers is not typical for Chlamydoselachus. His
ee Baie Text-figure 104.
work has been severely criticised, but in view of Ventral views of (A) heart and ventral aorta,
the marked variability that has been found in (B) valves of the conus arteriosus,
other organs and parts of Chlamydoselachus, it in Heptanchus maculatus.
seems possible that he worked on an anomalous 4b: aperture of last afferent artery; au., auricle (atrium);
5 ete . | al d t f iA fi br.af.1-6, first to sixth afferent branchial arteries;
specimen. ave include wo O 1s Hgures c.a., conus arteriosus; cr.I., left coronary artery; hy.af.,
(Text-figures 105 and 106), because of their his- afferent hyoidean artery; p.c., pericardial artery; v.a.,
$ ventral aorta; v.c., valves of the conus; vn., ventricle.
torical ump CuuaroIee and because they ENS jatose From Daniel, 1934, Fig. 150a and s; the latter redrawn
comprehensive than those of other authors. Atee Cagney 16M, 18, 1, ab SO.
THE ARTERIES
In Chlamydoselachus, particular interest attaches to the study of the dorsal aorta
(anterior portion), the branchial arteries, and the circulation within the gills.
THE Dorsat Aorta.—Ayers (1889) described a slender median artery, coursing
in the basis cranii, which he called the cranial aorta (c in Text-figures 105, 106, and 22
p. 352) since he regarded it as a direct continuation of the dorsal aorta. “Unlike all
other gnathostomous vertebrates, Chlamydoselachus has a dorsal aorta (dorsal vessel)
running the entire length of the notochord, to which it is intimately attached throughout
462 Bashford Dean Memorial Volume
S
f Nic-Z
wc (*
ieee cc.
EP == ke
$i iL z
GS s an
erry,
/ 2
Z us y
‘2
mas v: é cor.
va.
Text-figure 105.
Semidiagrammatic figure of heart and anterior blood vessels (anomalous?) of a specimen of Chlamydosel-
achus viewed from the left side.
a., auricle (atrium); a.i., anterior innominate artery; an., anastomotic branch of first efferent branchial artery; b.a., bulbus arteriosus;
br., brachial vein; c., cranial aorta; c. a., conus arteriosus; c.c., anterior carotid commissure; coe.mes., coeliaco-mesenteric artery; cor.,
coronary artery (plus hypobranchial trunk); c.s., cardinal sinus; c.v., cardinal vein; d.a., dorsal aorta (posterior to k.); e.c., external
carotid artery; h.v., hepatic vein; hy., hypophysis; ic., internal carotid artery; i.c.f., internal carotid foramen; i.j.v., internal jugular
vein; k., cephalic aorta; m.s., arteriae musculo-spinales; p.c.s., precaval sinus; p.pl., pituitary plexus; scl, subclavian artery; s.j.v.,
superior jugular vein; sp., spiracle; s.v., sinus venosus; tr., tropeic (lateral abdominal) vein; v., ventricle; v.a., ventral aorta; I-III,
first to third pairs of aortic roots (arches); 1-6, first to sixth pairs of efferent branchial arteries; 1!-6!, first to sixth pairs of afferent
branchial arteries.
After Ayers, 1889, Fig. 2.
Text-figure 106.
Efferent branchial vessels and dorsal aorta (anomalous?) of a specimen of Chlamydoselachus.
an., anastomotic branch of first efferent branchial artery; c., cranial aorta; coe.mes., coeliaco-mesenteric artery; d., dorsal aorta (posterior
to k.); e.c., external carotid artery; h., hyoid arch; i.c., internal carotid artery; i.c.f., internal carotid foramen; k., cephalic aorta; m.s.,
arteriae musculo-spinales; p.pl., pituitary plexus; scl., subclavian artery; sp., spiracle. I-IX, first to ninth pairs of aortic roots (arches);
1-6, first to sixth pairs of efferent branchial arteries; 1v—5v, first to fifth branchial arches.
After Ayers, 1889, Fig. 1.
The Anatomy of Chlamydoselachus 463
the greater part of its course” (Ayers, 1889, p. 195). Concerning the part of this vessel
which Ayers calls the cranial aorta, Allis (1908, pp. 111-112) comments as follows:
Ayers shows and describes, in Chlamydoselachus, a small median vessel, which runs
directly forward from the point where, according to his nomenclature, the dorsal aorta is
joined by the third pair of aortic roots; that is, in the nomenclature employed by me, from
the point where the lateral dorsal aortae unite to form a single median trunk. This vessel
Gy
K
o
=
SSeesonde
A
Scesccocoast
K\
;
Z
{
acr epsb apsb pehy
Text-figure 107.
The dorsal aorta and its branches in Chlamydoselachus, ventral view. The myelonic
(basilar) artery is displaced slightly to one side so as to be seen.
ab, arteria basilaris; acp, a. cerebralis posterior; acr, a. centralis retinae; aom, a. ophthalmica magna; apsb, afferent
pseudobranchial artery; da, dorsal aorta; ea 2-3, efferent arteries of second and third branchial arches; ec, external
carotid artery; epsb, efferent pseudobranchial artery; ic, internal carotid artery; Ida, lateral dorsal aorta; pehy,
posterior efferent hyal artery.
After Allis, 1923, Fig. 60, pl. XXIII.
is said by Ayers to extend forward to the pituitary body, and it is called by him the cranial
aorta, that being the name given by Hyrtl to a similar vessel said to have been found by him
in Scyllium. This median vessel, described in these two fishes, has been discussed by both
Dohrn and Carazzi, and there seems some doubt as to its existence; or, if it exists, as to its
being an artery. I have accordingly not given any consideration to it in my diagrams.
Further, Allis (1911, p. 516) states concerning the “cranial aorta” of Chlamy-
doselachus: ‘“No trace whatever of such a vessel could be found in either of my two
specimens, notwithstanding that it was most carefully and particularly looked for.”
Since the discredited concept of a cephalic or cranial aorta existing as a median
unpaired structure is of some historical importance, I append a further consideration of
it by quoting the following from Corrington (1930, pp. 227-228):
464
Bashford Dean Memorial Volume
This imaginary artery has been one of the causes operating to delay recognition of the
paired dorsal aortae. First described by Hyrtl (1872) in Catulus, its status and importance
were established by the author’s prestige. Later Ayers (1899) reported the same vessel in
Chlamydoselachus, seemingly to place this artery on a firm basis. But many other workers
have since been unable to find any trace of it whatever in any species, either in embryo or
adult. Dohrn attempted to explain Ayers’s paper but only confused matters the more, and
Text-figure 108.
The dorsal aorta (anterior portion) and its branches, also the first efferent branchial artery
and its branches, in Heptanchus maculatus.
ac., anterior cerebral; a.sp., arteria spinalis; br.ef.1, first branchial efferent; d.a.1, paired dorsal aorta; d.a., dorsal
aorta; hy.ef., hyoidean efferent; i.c., internal carotid; m.c., median cerebral; ns., nasal artery; o.m., ophthalmica
magna; or., orbital artery; p.c., posterior cerebral; ps., pseudobranchial artery; 7.a., ramus anastomoticus; 7s.,
rostral artery; sg., segmental artery.
After Daniel, 1934, Fig. 152.
it remained for Allis (1911.2) to re-examine the same species and to expose so many other
glaring errors in the previous work that Ayers’s description has been entirely discredited.
These paragraphs furnish the most striking case encountered in this investigation
illustrating the danger of (1) erecting specific types from the dissection of a single specimen;
(2) not making adequate allowance for a possible high degree of variability; and (3) attempting
to establish adult homologies without thorough embryological preparation.
The bifurcation of the dorsal aorta anteriorly, as portrayed in Text-figures 107, 108
and 109, of Chlamydoselachus, Heptanchus and Squalus respectively, is a feature common
to all elasmobranchs, so far as known. From an embryological point of view this is
The Anatomy of Chlamydoselachus 465
a primitive condition since, in the early embryo, the dorsal aorta is paired throughout
its entire length. As students of embryology know, the members of this pair of vessels
meet in the median line, throughout the greater part of their length, to form the single
dorsal aorta of adult anatomy. In gnathostomous vertebrates generally, the common
carotid and the internal carotid arteries are regarded as anterior portions of the primitive
dorsal aortae, which persist in the paired
condition throughout life. These consid-
erations lend interest to the study of these
arteries in Chlamydoselachus. My Text-
figures 107 and 110, after Allis, will en-
able the reader to follow the description
of these arteries which I quote from Allis
(1911, pp. 516-518) as follows:
Running forward and slightly later-
ally, immediately beneath the broad and
rounded base of the chondrocranium, the
lateral aorta [Ida] of each side is joined by
the corresponding efferent hyoidean artery
and then soon turns sharply laterally and,
at the edge of the base of the chondro-
cranium, receives the commissural vessel . . .
from the efferent hyoidean artery; thiscom-
missural vessel being considerably larger
than the lateral aorta. The latter vessel,
now becoming the common carotid, turns
sharply forward, at an acute angle, in the
direction prolonged of the commissural ves-
sel, runs forward and slightly mesially along
the lateral edge of the ventral surface of the
chondrocranium, and soon gives off its ex-
ternal branch... .
The internal carotid, which is the an-
terior prolongation of the lateral dorsal
aorta beyond the point of origin of the ex-
ternal carotid, runs forward and mesially
along the base of the chondrocranium and,
not far from the median line, traverses a
PA
Text-figure 109.
The carotid system of arteries in Squalus acanthias,
ventral aspect.
ACA, anterior cerebral artery; APA, afferent pseudobranchial
artery; BA, buccal artery; CA, cerebral artery; CC, carotid
crossing; CCA, common carotid artery; CS, cephalic sinus; DA,
dorsal aorta; DBCA, dorsal branchial commissural artery; EBA,
efferent branchial artery; ECA, external carotid artery; EHA,
efferent hyal artery; EPA, efferent pseudobranchial artery; ICA,
internal carotid artery; MCA, middle cerebral artery; OMA,
ophthalmic artery; PCA, posterior cerebral artery; PDA, paired
dorsal aorta; SA, segmental artery; SR, spiracular retia.
From Corrington, 1930, Text-fig. 22; after Hyrtl, 1872.
foramen in the base of the skull and enters the cranial cavity. ... Having entered the cranial
cavity, the internal carotid meets in the median line and anastomoses with, or is connected by
a short commissure with its fellow of the opposite side, and then immediately turns directly
laterally, and then forward and laterally in the cavity. There it is soon joined by the effer-
ent pseudobranchial artery, which artery enters the cranial cavity by traversing a foramen
in the orbital wall immediately anteroventral to the base of the eye-stalk. . . . Having
been joined by the efferent pseudobranchial artery, the internal carotid soon gives off an optic
branch and then separates into anterior and posterior cerebral branches, the latter of which
466 Bashford Dean Memorial Volume
fuses posteriorly, in the median line, with its fellow of the opposite side, to form a single
median myelonic artery. The optic artery issues from the cranial cavity with the nervus
opticus and penetrates the eyeball with or near that nerve.
My Text-figure 107 of Chlamydoselachus (after Allis) should be compared with
Text-figures 108 (after Daniel), and 109 (from Corrington, after Hyrtl), showing the
corresponding arteries for Heptanchus and Squalus respectively.
Tue BRANCHIAL ArTERIES.—Either Ayers’ (1889) figures (reproduced as my Text-
figures 105 and 106) are inaccurate, or his specimen of Chlamydoselachus was anomalous
om te
°P acer
: a
Text-figure 110.
Branchial, pseudobranchial and carotid arteries of Chlamydoselachus.
aal, II, etc., afferent arteries in the Ist, 2nd etc. branchial arches; acer, anterior cerebral artery;
ahy, afferent hyoidean artery; amd, afferent mandibular artery; apsb, afferent pseudobranchial
artery; cc, common carotid; cor., coronary; da, dorsal aorta; eal, II etc., efferent arteries in Ist,
2nd etc. branchial arteries; ec, external carotid; ehy, efferent hyoidean artery; epsb, efferent
pseudobranchial artery; ic, internal carotid; Ida, lateral dorsal aorta; om, arteria ophthalmica
magna; op, optic artery; pcer, posterior cerebral artery; psb, pseudobranch; ta, truncus arteriosus.
After Allis, 1911, Fig. 1.
in this respect: only one efferent-collector artery is shown in each gill-arch, whereas in
all other specimens of Chlamydoselachus that have been examined, my own specimens
included, there are two such arteries. To be sure, Goodrich (1909, p. 137) wrote: ““Ex-
cept in Chlamydoselachus, the branchial arches of the Selachii, like those of the Dipnoi,
have two efferent arteries; but it is probable that Goodrich merely accepted Ayers’
account without verifying it. In his later (1930) text, Goodrich figures Chlamydoselachus
with two efferent arteries in each gillarch. Allis (1908) at first accepted Ayers’ de-
scription of the efferent branchial arteries, but later (1911) he prepared a figure (my
Text-figure 110) based on dissections of his own material, and commented (pp. 511-512)
on the results as follows:
The Anatomy of Chlamydoselachus 467
In 1889 Ayers, in a work entitled “The Morphology of the Carotids,” described the
branchial and carotid arteries in Chlamydoselachus, and these arteries, as described by him,
were in certain respects quite unusual. Ayers himself called especial attention to this fact,
and on the conditions, as described by him, he based certain quite important conclusions.
In 1908 I had occasion to consult this work by Ayers, and I then published (Allis, 1908) a
diagrammatic representation of the carotid and related arteries in this fish, as described by
Ayers but as interpreted by myself. The diagram was, however, most unsatisfactory, and
0) om pcer ec epsb
acere : A, Hay daar
PSO apsb ely eall call da
C3 Ida : Brae Bae ae :
Text-figure 111.
Branchial, pseudobranchial and carotid arteries of Heptanchus cinereus.
aal, II, etc., afferent arteries in the lst, 2nd etc. branchial arches; acer., anterior cerebral artery;
ahy, afferent hyoidean artery; amd, afferent mandibular artery; apsb, afferent pseudobranchial
artery; cor, coronary artery; da, dorsal aorta; ea.I.II. etc., efferent arteries in the 1st, 2nd, etc.
branchial arches; ec, external carotid; ehy, efferent hyoidean artery; epsb, efferent pseudo-
branchial artery; ic, internal carotid; ilh, internal lateral hypobranchial artery; Ida, lateral dorsal
aorta; om, ophthalmica magna artery; op, optic artery; pcer, posterior cerebral artery; psb,
pseudobranch; ta, truncus arteriosus.
After Allis, 1912, Fig. 1.
having since received several heads of this fish, most kindly sent me by Prof. Bashford Dean,
I have had dissections made of the arteries concerned, in two of them, the dissections being
prepared by my assistant, Mr. Jujiro Nomura. The arteries, as I find them, are shown in
the accompanying Figure 1 [my Text-figure 110]. ...
The arteries in Chlamydoselachus . . . differ in no important particular from those in the
Scylliidae and in Mustelus (Allis, 1908), excepting in that the dorsal end of the efferent
hyoidean artery has, in Chlamydoselachus, a double connection with the lateral dorsal aorta.
In Chlamydoselachus, as in elasmobranchs generally, the efferent-collector arteries
(Text-figure 110) form complete loops around each gill-cleft excepting the last one. To be
468 Bashford Dean Memorial Volume
sure, Ayers notes the absence of such loops in his specimen, but they are shown in
various figures by Allis (1911 and 1923). In Chlamydoselachus a posterior efferent-
collector may retain a dorsal connection with the anterior efferent-collector of the same
gill (Text-figure 110), an arrangement not usually found in adult elasmobranchs though
commonly present in their early embryos.
As portrayed in Text-figure 110, the afferent branchial arteries of Chlamydoselachus,
excepting the hyoidean and the last branchial, bifurcate dorsally, one branch passing
over the cleft anteriorly to join the afferent in front, the other passing posteriorly over
the succeeding cleft to join the following afferent. Thus the afferents, like the efferents,
are connected into a series of loops around all the clefts. Complete afferent loops are not
found in other sharks. Basing his opinion upon what is known concerning the manner
of development of the branchial arteries in other sharks (particularly in Squalus as de-
scribed by Scammon, 1911), Corrington (1930) concluded that the anastomoses which
complete the afferent loops around the gill-clefts in Chlamydoselachus could arise only
late in embryonic development, after the arterial pattern had been nearly completed;
therefore they are among the most recent acquisitions of the branchial arches. They
represent a secondary and specialized condition—an interpolation—in Chlamydoselachus,
and are probably incipient in Heptanchus (Text-figure 111).
In elasmobranchs generally, each epibranchial artery of the early embryo is situated
dorsal to a gillarch; but in later development these arteries become shifted to positions
dorsal to the respective gill-slits (Goodrich, 1930, Figs. 531a—p and 532). In Chlamy-
doselachus, the epibranchial arteries of the adult (Text-figure 110) are situated dorsal to
the respective gillarches—that is, they retain what is presumably their embryonic
position. According to Allis (1912) they are very nearly in the same position in Heptan-
chus (my Text-figure 111).
Corrington (1930, p. 198) suggests that, since Daniel has given us the apt desig-
nation of efferent-collector artery for the lower forks that gather up the oxygenated blood
from the gills, we may restrict the name efferent branchial artery to the upper and single
trunk, thus expressing its revehent correspondence to the afferent branchial artery in
their relationships to the gills. Epibranchial thus becomes a synonym for efferent bran-
chial. Concerning the efferent branchial (epibranchial) arteries in elasmobranchs,
Corrington (pp. 198-199) writes as follows:
The first of the series is the efferent hyal artery which courses forward and has been . . -
long identified with the carotid system. . . . Then follow 4, 5 or 6 efferent branchials, de-
pending on the species, and conforming to the number of gills and of afferents, as previously
noted. Usually these are all separate, but in Notorhynchus, Heptranchias [Heptanchus],
Chlamydoselachus and doubtless in other notidanids, the last efferent joins the penultimate
midway of its course so that the two have a common stem thence to the aorta. The condition
indicates the approaching loss of the last gill in each case, and is a parallel circumstance to
the fusion of the pharyngobranchials of the last two skeletal arches, so commonly seen in
sharks.
The Anatomy of Chlamydoselachus 469
ARTERIOLES WITHIN THE Gitts.—In searching the literature on Chlamydoselachus,
Ihave found nothing on the blood-vascular system within a gill proper. In order to study
this I have been obliged to prepare serial sections of gillarches and holobranchs excised
from my specimens.
The general plan of the blood-vascular system within a gill is indicated in my Text-
figures 78, 79 and 80 (see pages 421 and 422), which do not, however, show any capil
Text-figure 112. Text-figure 113.
Sections through gills of elasmobranchs, showing afferent and efferent vessels.
Text-figure 112. Section across gill-bar of Scyllium canicula, late embryo 32 mm.
long, showing blood supply to lamellae.
aef, anterior efferent artery; af, afferent artery; al, anterior lamella (filament); b, branchial bar; em,
external constrictor muscle; gr, gill-ray; grk, gill-raker; im, adductor branchialis muscle; n, nerve;
pef, posterior efferent artery; pl, posterior lamella (filament) continued intc external filament (not
present in adult); s, gill-septum.
After Goodrich, 1930, Fig. 516.
Text-figure 113. Diagram illustrating the structure of a gill of a selachian.
aef, anterior efferent artery of arch; af, afferent artery of lamella (filament); al, anterior lamella (fila-
ment); gr, gill-ray; lm, capillary network; pef, posterior efferent artery; pl, posterior lamella (filament);
prn, pretrematic nerve; prnd, branchial muscle; ptn, post-trematic nerve; s, outer region of septum;
sc, superficial constrictor muscle; sk, skeletal arch.
After Goodrich, 1930, Fig. 517p.
laries. An afferent artery, (af. br.a. in Text-figure 78), coursing along the outer side of
the gillarch, gives off a branch (afferent branchial arteriole) to each filament. Each
afferent arteriole passes along the base of the corresponding filament (Text-figure 78),
giving off numerous branches to it (Text-figures 79) and also to the septum. The precise
manner of this branching has not been fully worked out, since the task requires an elabo-
rate reconstruction, but it is evident that many of the arterioles are here somewhat
lacunar in character. An efferent branchial arteriole (ef. br. a. in Text-figure 78) courses
along the outer edge of each filament, returning the blood from the capillaries of the
filament to an efferent-collector artery of the gillarch. A fairly large vein, (v. in Text-
470 Bashford Dean Memorial Volume
figure 78), presumably draining the blood from smaller vessels in the gill-septum, was
found in the proximal portion of the septum. Just proximal to the main afferent artery
of the gill-arch, in the location where an extension of the coelomic cavity presumably
occurs in the early embryo, there is a fairly large space which probably represents a
lymphatic vessel whose thin wall is incompletely preserved.
The distribution of arteries within a gill of Chlamydoselachus is essentially the same
as in other elasmobranchs, e. g., as in Heptanchus (Text-figure 81, p. 423); in Scyllium
(Text-figure 112); and in selachians generally (Text-figures 113 and 114). Of these
figures, Corrington’s (my No. 114) is the only one showing an intermediate branchial
CAA GR
AN Pot
ABA STC! FECA
/BCA
Text-figure 114.
Frontal section through a shark-gill, drawn semidiagrammatically.
ABA, afferent branchial artery; ABAr, afferent branchial arteriole; AdA, adductor arcuus; AECA, anterior efferent-
collector artery; AGF, anterior gill-flament; Cb, ceratobranchial; CSf, constrictor superficialis; CT, connective tissue;
EBAr, efferent branchial arteriole; ExbA, extrabranchial artery; ExbC, extrabranchial cartilage; GR, gill-ray, distal portion
not shown; GRR, gill raker; GS, gill-septum; Ib, intrabranchialis; IBCA, intermediate branchial commissural artery; PECA,
posterior efferent collector artery; PGF, posterior gill-flament; Pot, post-trematic ramus, branchial nerve; Prt, pretrematic
ramus, branchial nerve; VNBV, ventral nutrient branchial vein.
After Corrington, 1930, Fig. 10, p. 200.
commissural artery (IBCA) connecting the two efferent-collector arteries of a single gill.
Such arteries exist in Chlamydoselachus (Text-figure 110) as well as in many other elasmo-
branchs. In some of my sections, I have observed a small artery in the appropriate
location for an intermediate commissural artery but was unable to trace its connections
due to the lack of a sufficient number of sections in the series.
The gill-filaments of Chlamydoselachus contain few capillaries; they consist chiefly
of connective tissue traversed by arterioles and bounded by a very thin integument.
They serve, therefore, mainly as supports for the lamellae which are the essential organs of
respiration. The lamellae are exceedingly rich in capillaries. In a section, such as that
shown in outline in my Text-figure 80 (p. 422), most of the capillaries are cut trans-
versely. Since the lamellae are only slightly thicker than the capillaries when the latter
are distended with blood (as they usually are in my sections), each capillary comes in
contact with the integument on two sides. So rich is the capillary plexus that there
is scarcely any space between capillaries; in sections where the capillaries are cut trans-
versely they look somewhat like a string of beads.
The Anatomy of Chlamydoselachus 471
In studying the blood-vascular system of the gills of Chlamydoselachus, one is
impressed by the enormous increase in the cross-sectional area of the blood stream as it
leaves the gill-arch, as it enters the filaments, and again as it reaches the plexus of capil-
laries in the lamellae. There is a corresponding decrease as the blood returns to the main
efferent branchial arteries. The total arrangement functions to reduce the velocity of
the blood as it passes through a multitude of tiny capillaries.
In the section on the respiratory system I have pointed out that in proportion to
body size the respiratory surface in Chlamydoselachus is very large—perhaps larger than
in most sharks. It seems likely that in fishes that live in the deeper waters of the ocean,
where it is always cold and where oxygen is not so plentiful as at the surface, there
is need for more efficient organs of respiration; but adequate data for comparison are
not available.
In his well-organized treatise on the anterior arteries of sharks, Corrington (1930)
gives a refreshingly clear presentation of the essential data, illuminated by discussions
of its significance from a comparative point of view. His synonymy for these arteries
will be found very useful. Some remarks by Corrington (p. 205) on the hypobranchial
system of arteries will perhaps explain why I have not included a comparison of these
vessels in Chlamydoselachus with those of the same region in other sharks:
These [hypobranchial arteries] are the last arteries of the head to be formed before
assumption of the.adult condition. This lateness of development and also absence in lower
groups argue that this system was one of the last vascular acquisitions of the immediate
shark ancestor. Increased bulk and muscular specialization of the subpharyngeal, inter-
branchial area demanded an extra mechanism for nutritive supply, and this was hence derived
from the nearest source. No homologies involving the alteration of any elements previously
present are necessary or possible, and none have been suggested as far as I am aware.
There is no type arrangement for these arteries in either the Class or Order, or even in various
species, so that description must be of a somewhat general nature.
The most elaborate figures of the arteries of the head of Chlamydoselachus are those
of Allis (1923). These (which are in color) should be consulted by any one wishing a more
comprehensive account than is given here.
THE VEINS
Very little work has been done on the venous system of Chlamydoselachus. Ayers
(1889) states that extensive venous sinuses, always simple in character, are developed
in the course of the large venous trunks. Portions of the principal venous trunks are
shown in Text-figure 105, copied from Ayers. These vessels are the internal jugular
vein (i.j.v.), the cardinal vein (c.v.), the hepatic vein (h.v.), and the tropeic or lateral
abdominal vein (tr.). The cardinal sinus (c.s.) seems unusually large, as in my own speci-
mens. The marked development of the venous sinuses is regarded by Ayers as a primitive
character.
472 Bashford Dean Memorial Volume
Hawkes (1906, p. 983) states that in Chlamydoselachus the anterior cardinal vein
lies in the vicinity of the vanished seventh gill-cleft, though in most elasmobranchs it is
in the position of the missing sixth gill-cleft.
The claspers of Chlamydoselachus have been studied comprehensively by Leigh
Sharpe (1926). His Fig. 5a-c (my Text-figure 115a—c) shows the endoskeleton, certain
muscles, and the venous sinuses of the claspers. His Figures 5a and B have been referred
to in the sections on the endoskeleton (p. 376) and muscular system (p. 395) respectively.
The venous sinuses of the claspers of Chlamydoselachus are described by LeighSharpe
(1926, pp. 312-313) as follows:
The main blood-vascular system is composed of
two venous sinuses, parallel to, and on either side
of, the myxapterygium (Fig. 5c) [Text-figure 115c],
in connection with which no erectile tissue could
be discovered.
The inner [sinus], which is the longer and more
superficial (Figs. 4a [my Text-figure 97a, p. 452] and
5c [my Text-figure 115c]), arises posteriorly in the
distal third of the clasper, and, surrounding the
clasper muscles, ends blindly in the middle line
anterior and ventral to the cloaca. Dorsal to the
myxapterygial articulation it communicates with
the other, more lateral, deep-seated sinus; the latter
drains blood from the extra-cloacal region and from
the edges of the clasper and, continuing forward,
Text-figure 115. empties its contents into the iliac vein dorsal to the
Claspers of Chlamydoselachus in ventral as‘ basipterygium. Five nerves, proceeding to the pel-
pect: A, the cartilages; B, the musculature; vic fin and clasper, traverse this sinus, and also a
and C, the venous system of the clasper. space (apparently lymphatic) between it and the
a.m., anteroflexor muscle; Ap., position of apopyle; abdominal muscles. These structures are seen dis-
oe ey See aS. aaa ee “*= played in Fig. 48 [my Text-figure 97s, p. 452], and
After Leigh-Sharpe, 1926, Fig. 5. the entire venous system in Fig. 5c [my Text-figure
115c]. As stated above, the function of the blood-
vascular system in Chlamydoselachus does not appear to be that of erection, nor would the
metabolism of the muscles supplied by it warrant so extensive a system of vessels. Possibly
the sinuses are required to provide easy play for the muscles in the position of antero-flexion.
THE NERVOUS SYSTEM
Although some careful work has been done on the nervous system of Chlamydo-
selachus, much remains to be accomplished before a satisfactory account can be written.
The brain has never been adequately described, even superficially, and the spinal cord
has been ignored. The functional analysis of the cranial and spinal nerves is incomplete.
Save for some references to the ciliary ganglion, the sympathetic system has been wholly
neglected. Lack of time and suitable material prevents my attempting to remedy any of
these deficiencies.
The Anatomy of Chlamydoselachus 473
THE BRAIN
Garman’s brief description (1885.2, pp. 16-17) of the brain of Chlamydoselachus,
illustrated by his Pls. XV and XVI (my Plate VI) is the first, and remains the most
comprehensive account of the form and structure of this organ. This comparative neglect
may be partly explained by the fact that it appears to be very difficult to obtain specimens
in which proper attention has been given to the preservation of the brain. Garman
states that the brain of his specimen was very soft. When removed from the skull, it
collapsed and spread out, so that the figures sketched are a trifle more broad and flattened
than is natural. His entire description follows:
The brain is very small. Comparatively the amount of forebrain is much smaller than
in the higher sharks, Carcharias, Zygaena, and others. In outlines and proportions there is
great similarity between this brain and that of the Notidanidae. In both of the genera of
that family the brain is equally elongate and the disposition of the nerves is not greatly
different; the differences are mainly in details rather than in general build. ... The olfactory
lobe is shorter than that of Hexanchus (compare Maclay, Das Gehirn der Selachier, Plate
II). The olfactory bulb is similar in shape in these genera; it is a club-shaped expansion
with lobules at the end from which the nerve distribution takes place. Being broader in
front, the hemispheres taper more toward the hypophysis than is the case in Hexanchus. As
in the latter, the optic lobes are rounded above and in front, and are—when viewed from _
above—about half exposed.
The cerebellum is of medium size, rather smooth on its upper surface, rounded in front,
and presents an acute angle—with blunted apex—between the corpora restiformia. On the
upper surface the longitudinal depressions are partly due to the uneven floor of the ventricle,
on which the upper walls rest. There are three moderate transverse depressions. In the
cerebellum the amount of plication is greater than that in Hexanchus as figured by Maclay.
There is some likelihood that his figure is taken froma young specimen, and that a large one will
be marked by greater complication. In Maclay’s figure of Hexanchus the folds are represented
by a simple upward line with a transverse bar on the top, like a letter T. To represent the
same section in the new shark, we shall have to place another T on each end of the transverse
bar. Maclay figures a longitudinal section of the cerebellum of a young Mustelus, which
shows a pretty close agreement. An adult Mustelus, which is a great deal more complex,
is also figured.
The corpora restiformia are comparatively large; they approach each other behind the
cerebellum till there is but a small space between them.
The medulla is large, somewhat larger than the same portion in the Notidanidae. The
waved appearance in the sinus rhomboidalis, fourth ventricle, is caused by the transverse
bands of fibers in its membranous roof. . . .
The close similarity existing between the brains of Chlamydoselachus and the Notidan-
idae is a strong point in favor of genetic relationship.
From the report on an address by Wilder (1905) before the American Philosophical
Society, I quote the following:
Here [in Chlamydoselachus] the walls of the forebrain are thinner and less differen-
tiated [than in Scymnus], and in the lateral extensions toward the olfactory cups (‘nostrils’) the
so-called cerebral portion expands nearly equally in every direction from the axis represented
by the olfactory crus; in most other sharks and in rays or skates the special cerebral extension is
474 Bashford Dean Memorial Volume
toward the meson or middle line, so as to meet the corresponding part of the other side; in
the lamprey the cerebral extensions are away from the meson; in the Dipnoi, as shown by the
speaker in 1887, they are downward, while in the ordinary and higher air-breathing verte-
brates, reptiles, birds and mammals, the cerebral hemispheres expand mostly upward. It
is as if nature had experimented in the four directions at right angles with one another from
the primitive condition, nearly as in Chlamydoselachus, where the extension is almost uni
formly in all directions from the olfactory axis. .. . In this connection the speaker reiterated
his previously expressed conviction that in evolution the olfactory portion of the brain had
preceded the cerebral; that the ancestral vertebrates needed to smell rather than to think;
that the organ of forethought had been, so to speak, an afterthought, and that the cerebral
region, so preponderant in man, was rather an offshoot from the olfactory region, and had
been interpolated between that and the hinder portions of the brain.
Hawkes’ (1906) figures (my Figures 13 and 14, Plate IV) representing dorsal and
ventral views of the brain of Chlamydoselachus are not well adapted for showing the
form of the brain, since each figure shows only a lateral half and some parts have been
cut away. In general, the brain appears broader and shorter than in the other figures,
and the breadth is particularly noticeable in the region of the medulla. Hawkes’ descrip-
tion (p. 987) of the brain follows:
The external features of the brain [of Chlamydoselachus] having a typical arrangement,
need not be described. . . . Two points only may be noticed: (1) there is a large rhinocoel
extending to the end of the olfactory stalk; (2) the dorsal roof of both prosencephalon and
thinocoel is non-nervous. This second point is of considerable interest, as it recalls the
condition of Ammoccetes and of the teleosts. The non-nervous roof may be regarded as prim-
itive when compared with that of Ammocoetes, but as specialized when compared with
that of the Teleosts. That a non-nervous roof should be found among the Elasmobranchs
is a point of considerable interest, although its significance is as yet undetermined.
It is not clear whether Hawkes made a microscopical examination of the roof
described as non-nervous; she states merely that this observation was made on an
immature specimen.
Allis’s (1923) artistic portrait of the brain of Chlamydoselachus is reproduced as
my Figure 7, plate III. This figure gives the impression of being accurately drawn from
a well-preserved specimen, and is evidently not in any sense a diagram. It should be
explained that the membranes enclosing the brain had not been removed. Allis states
that this dissection had not been completed nor controlled when work was stopped by
the death of his assistant, Mr. Nomura. Comparison of this figure with Daniel’s (1934)
figure representing a dorsal view of the brain of Heptanchus (reproduced as my Figure
28, plate VII), gives point to Garman’s remark that the brain of Chlamydoselachus
closely resembles that of a notidanid. In Allis’s figure, the optic lobes seem considerably
smaller, and the cerebellum larger, than in Heptanchus. The olfactory lobes are longer
than those of Heptanchus, though Garman says that they are shorter than those of Hexan-
chus. These comparisons are of course based on the proportional size of each part in
relation to the total size of the brain. The olfactory tracts diverge more strongly in
Chlamydoselachus than they do in Heptanchus.
The Anatomy of Chlamydoselachus 475
Concerning the source of his material for study
of the cranial anatomy of Chlamydoselachus, Allis
(1923, p. 123) wrote as follows:
In 1902, Professor Bashford Dean, of Columbia
University, New York City, most kindly sent me a
single head of Chlamydoselachus, and it was given to
my assistant, Mr. Jujiro Nomura, for dissection. It
was, however, soon found that this one head would
not suffice for the work contemplated, and, at my
request, Professor Dean had several other heads sent
me from Japan.
Inall the figures of the brain of Chlamydosela-
chus, the divisions are very incompletely labeled.
To one familiar with the structures of the elasmo-
branch brain, the parts are readily recognizable. In
any event they may be identified by reference to
my Figure 28, plate VII, and to Text-figure 116,
after Daniel, representing dorsal and ventral views
of the brain of Heptanchus, which is very similar
to that of Chlamydoselachus.
Today, there are available for comparison a
wealth of figures of the elasmobranch brain that
were not in existence when Garman wrote his
description of the brain of Chlamydoselachus.
Particular mention should be made of the many
fine drawings of selachian brains published, much
later, by Garman (1913) himself. These, buried
in his great systematic monograph on “The Pla-
giostomia,” have probably never received the at-
tention that they deserve. They do not, how-
ever, include figures of the brain of Chlamydosel-
achus nor of any notidanid.
THE CRANIAL NERVES
Text-figure 116.
The brain and cranial nerves of Heptanchus
maculatus in ventral view.
bu. VII, buccal branch of facial nerve; di., dien-
cephalon; hmd., hyomandibular division of the facial
nerve; il., inferior lobe; med., medulla; ms., mesen-
cephalon; md.V, mandibular division of the fifth or
trigeminal nerve; mx.V, maxillary division of the
trigeminal; os. VII, ophthalmicus superficialis division
of the facial nerve; tl., telencephalon; v.s., vascular
sac; w. to z., occipitospinal nerves; II, III, IV, VI,
IX and X, cranial nerves.
After Daniel, 1934, Fig. 200s.
Garman’s (1885.2) account of the cranial nerves of Chlamydoselachus is limited to
naming them and to describing, in a very general way, the superficial origin of their
roots. Hawkes (1906) has given us the only comprehensive and detailed account of the
entire series of cranial nerves; her illustrations of these nerves are reproduced herein.
476 Bashford Dean Memorial Volume
Brohmer (1909) described briefly the cranial nerves of a 25-mm. embryo. The account of
the cranial nerves by Allis (1923) is, as the author states, incomplete.
The general plan of the cranial nerves of vertebrates is best revealed in their em-
bryos. For the embryo of Scylliwm, this plan is set forth diagrammatically in Text-figure
117. A somewhat comparable figure for Chlamydoselachus, based on a single embryo,
is supplied by Text-figure 118, after Brohmer.
Text-figure 117.
Diagram of the segmentation of the head in an embryo of Scyllium canicula. The myotomes are
longitudinally striated, the nerves black, and the scleromeres dotted. The cartilaginous visceral
arches, also the optic capsule and the nasal sac, are represented by dotted outlines.
LVI, gill-slits; 1-11, somites, prootic from 3 forwards, and metaotic from 4 backwards; a, auditory nerve; ab, abducens nerve;
ac, auditory capsule; ah, anterior head cavity; c, coelom in lateral plate mesoblast; cr, limit of cranial region; f, facial nerve;
gl, glossopharyngeal nerve; ha, hyoid cartilaginous arch; hm, hypoglossal muscles from myotomes of somites 6, 7, 8; hy,
hypoglossal complex nerve; la, lamina antotica; m, mouth; m2, second metaotic myotome; m6, sixth metaotic myotome;
ma, mandibular cartilaginous arch; mb, muscle bud to pectoral fin; nc, nasal capsule, continuous with trabecula behind;
aal and aa2, first and second occipital arches of segments 6 and 7; om, oculomotor nerve; prf, profundus nerve; scl, sclerotome
of segmentl10; sp1, vestigial dorsal root and ganglion of first spinal nerve; sp2, second spinal; t, trochlear nerve; te, trigem-
inal nerve; v, complex root of vagus nerve; vgl, vestigial dorsal root and ganglion of segment 7; vc, ventral coelom extending
up each visceral bar; vr, ventral nerve root of segment 6, supplying second metaotic myotome and hypoglossal muscle;
vs, limit of visceral region.
After Goodrich, 1918.2, Text-fig. 1.
For the adult Chlamydoselachus, the chief cranial nerves are represented in my
Figure 29, plate VII. The roots of the cranial nerves are shown in Figures 13 and 14,
plate IV, and in Text-figure 119. For comparison, I have inserted a figure showing the
cranial nerves of Squalus (Text-figure 120). My principal illustration of the cranial
nerves of Chlamydoselachus (Figure 29, plate VII) is complicated by a diagram of the
lateral line system of sensory canals. Hawkes, throughout her work on Chlamydoselachus,
The Anatomy of Chlamydoselachus 477
devoted much attention to the innervation of the lateral line system, renaming most of
the divisions of that system in accordance with their nerve supply—a method first
employed by Cole (1896) in his work on Chimaera, and which has since been generally
adopted.
The reader who is not familiar with the terms employed in the classification, on
a functional basis, of the cranial nerve components of fishes should consult Herrick,
1899, pp. 7-19; Johnston, 1905.1, pp. 176-184 and Pl. IV; Norris and Hughes, 1920,
Fig. 51, showing the cranial nerve components of Squalus in color; and Goodrich, 1930,
pp. 725-755.
A complete résume of the rather lengthy descriptions, by Hawkes (1906) and Allis
(1923), of the cranial nerves of Chlamydoselachus seems unnecessary since, for the most
part, these nerves are much like those of other elasmobranchs (e.g., Heptanchus, briefly
described by Daniel, 1934; and Squalus, elaborately described by Norris and Hughes,
1920). It seems sufficient to mention some respects in which the cranial nerves of Chlamy-
doselachus are more or less unique, or in which the descriptions of authors differ. The
following account is based primarily on Hawkes’ description.
A nervus terminalis is not mentioned by Garman, nor is it shown in any of his
figures of the brain. It is, however, described by Hawkes (who calls it Locy’s nerve,
L.N., Figure 13, plate IV) as large and well-defined. Originating near the median line,
somewhat to the ventral side of the forebrain, it passes outward, curving upward along
the anterior and upper side of the olfactory stalk to be distributed between the end of the
stalk and the beginning of the olfactory capsule. .On reaching this point, the nerve
becomes somewhat enlarged by flattening, then breaks up into a number of fine branches
which pass toward the olfactory epithelium but could not be traced to their endings.
Allis (1923) writes that in his specimen a small nervus terminalis runs outward
along the anterior surface of each tractus olfactorius, and then turns upward onto its
dorsal surface, as stated by Hawkes. The terminal portion of the nerve of the left side
is shown (without a label) in Figure 7, plate III.
The olfactory nerve of Chlamydoselachus is neither figured nor mentioned by any
author. From this we may surmise that it is essentially the same as in other elasmobranchs,
developing from neuroblasts in the epithelium of the olfactory capsule and extending as
a double nerve backward to the olfactory bulb. In Heptanchus, as in some other forms,
the nerve is so short as to be hardly recognizable without microscopical examination.
The optic nerve (2, Figures 25, 26 and 27, plate VI, after Garman) does not take
the most direct route to reach the eyeball. As described by Allis (1923) and as shown in
his Figs. 52 and 59 (the latter reproduced as my Figure 7, plate III) this nerve runs antero-
laterally. Having issued through its foramen, it turns ventro-latero-posteriorly around
the anterior end of the capsular sheath that encloses the orbital process of the palato-
quadrate, and reaches the eyeball, passing ventral to the somewhat ligamentous portion
of the connective tissue that attaches the capsular sheath to the anterior wall of the orbit.
478 Bashford Dean Memorial Volume
The innervation of the muscles that move the eyeball is shown (with the exception
of the abducens or sixth nerve, which innervates the external rectus) in my Figures
10, 11 and 12, plate IV. The chief peculiarities of the muscles (p. 392, Text-figures 66 and
67) are: (1) the external rectus is divided, as in some other elasmobranchs, into two
parts; and (2) all the recti muscles are attached to the top of the eyestalk, near its flat-
tened head. Allowing for these peculiarities of the muscles, the distribution of the third
(oculomotor), fourth (trochlear), and sixth (abducens) nerves is the same as in vertebrates
generally. The relations of these nerves are described by Allis (1923).
Hawkes states that only one root of the trigeminal nerve (R.V. in Text-figure
119a and B) is recognizable macroscopically, though presumably both sensory and motor
components are present as in other forms. The single root is broad, but in a side view
it is almost completely hidden by the ganglion buccalis (VII in Text-figure 119a and B).
The ophthalmicus profundus nerve (Pro.), together with the ophthalmicus super-
ficialis V (S.Op.V.), originates from a small enlargement (presumably ganglionic) on the
inner side of the Gasserian ganglion (V in Text-figure 119s). Thus, as in Chimaera
(Cole, 1896) and in Petromyzon (Johnston, 1905.2), there is evidence that, at the present
time, the profundus (prf.) is a branch of the trigeminal, although in origin it belongs to
a more anterior segment (Johnston, 1905.1), as shown for Scyllium in Text-figure 117.
In both Chimaera and Petromyzon, the profundus nerve has an undoubted ganglion.
The distribution of this nerve is described by Hawkes (1906, p. 971) as follows:
On entering the orbit the [profundus] nerve passes between the large rectus externus
muscle and the cranial wall, sending dorsally a long ciliary nerve which ends around the
upper part of the eyeball. The main nerve then passes outward, parallel with the oculomotor
nerve, to which it sends or from which it receives an anastomosing branch. Five mm. beyond
the origin of the ciliary branch the profundus passes somewhat ventrally between the eyeball
and the external rectus muscle to disappear in the eyeball, near the point of insertion of the
ventral part of the external rectus muscle. The profundus passes for about 1 cm. under the
covering membrane of the eyeball, emerging near the point where the optic nerve originates
from the eyeball. The nerve then passes anteriorly and out of the orbit immediately to the
outer side of the attachment of the inferior oblique muscle. Almost at once the nerve divides
into a number of branches, which spread over the olfactory capsules immediately below
the skin.
The course of the profundus nerve in the region of the eyeball is illustrated in
Figures 10 and 12, plate IV, after Hawkes, who suggests that the anastomosis (A.B.)
between the profundus and the oculomotor nerve may comprise the fibers that connect
the ciliary ganglion and the oculomotor nerve, which here pass not directly to the ciliary
ganglion, but by way of the profundus. The distribution and relations of the profundus
nerve in the region of the eyeball are described in more detail by Allis (1923).
Brohmer (1909) states that in his 25mm. embryo of Chlamydoselachus the ciliary
ganglion occurs in the course of the nervus ophthalmicus profundus, which sends a branch
to the ‘‘nerve knot” on the wall of the premandibular cavity (Text-figure 118). From the
nerve knot a branch, which Brohmer calls the oculomotorius (Oc.), extends forward.
The Anatomy of Chlamydoselachus
He was unable to trace this nerve to the brain.
479
In his summary (p. 677) he writes:
“Der Oculomotorius steht mit dem Trigeminus in Verbindung.”
Ziegler (1908) remarks that the 25mm. embryo of Chlamydoselachus studied by
his pupil, Brohmer, was cut in “eine luickenlose Schnittserie.” Ziegler’s account of the
cranial nerves of Chlamydoselachus, which is based on Brohmer’s studies and some
observations of his own, is largely a confirmation of Brohmer’s results. Ziegler evidently
believes that, in elasmobranchs generally, the ciliary ganglion is closely associated with
the profundus nerve, though many authors have emphasized its relation to the oculomotor.
In various selachians, one or more
small (ciliary) ganglia are related to the
oculomotor nerve (Daniel, 1934). These
ganglia give rise to nonmedullated fibers
which make up the short ciliary nerve. In
Squalus (Norris and Hughes, 1920) the
ciliary ganglion is connected by fibers
with the oculomotorius, the ophthalmicus
profundus V, and the palatinus VI/ nerves.
A review of the literature on the relations
of the ciliary ganglion in elasmobranchs is
given by Norris and Hughes (1920).
In Chlamydoselachus the superficial
ophthalmic V, according to Hawkes,
passes from the Gasserian ganglion side
by side with the profundus nerve, which
it equals in size. It at once passes dorsally
and enters the same groove as the oph-
thalmicus superficialis VII, with which,
however, it does not unite. About as far
forward as the external nares, but nearer
the median line, it spreads out into many
branches which lie immediately under the
skin. This nerve apparently contains only
cutaneous elements. A somewhat differ-
ent account of the same nerve is given by
Allis (1923, pp. 210-211) as follows:
The ramus ophthalmicus superficialis
trigemini, as I define this nerve, includes the
similarly named nerve of Merritt Hawkes’
descriptions and her ramus ophthalmicus
superficialis facialis, and these two nerves
were completely fused with each other in
the two specimens examined, instead of
Text-figure 118.
Reconstruction of the cranial nerves in a 25-mm.
embryo of Chlamydoselachus.
Ac., nervus acusticus; Cg., ciliary ganglion; D.e., ductus endolym-
phaticus; F.Ac., n. facialis acusticus; Ggl.1, Ggl.2, remnants of
the ganglionic crest; Gl., n. glossopharyngeus; Gl.v., ventral root
of the glossopharyngeal nerve; N.l.v., n. lateralis vagi; Oc., n.
oculomotorius; 4, nerve knot in the premandibular cavity; R.bucc.,
ramus buccalis; R.hy., ramus hyoideus; R.md., ramus mandibularis;
R.mx., ramus maxillaris; R.o.s., ramus ophthalmicus profundus;
Spr. (I)., spiracle (first gill-cleft); I7., n. trigeminus; Vg., roots of
the vagus nerve; Vg.5., the last branch of the vagus; 1.Sp., first
spinal ganglion; 1.v., first ventral root (of the occipitospinal
nerves); II, II, IV, V, second to fifth gill-clefts.
After Brohmer, 1909. Text-fig. 10.
480
1923).
Bashford Dean Memorial Volume
being wholly independent, as Merritt Hawkes describes and shows them. Further-
more, it is to be noted that the origin of her ophthalmicus superficialis trigemini from that
small swelling on the inner side of the Gasserian ganglion from which the ophthalmicus
profundus has its origin, would seem to indicate that it is a portio ophthalmici profundi
and not a trigeminus nerve, and its origin in Squalus, as given by Landacre (1916), and its
distribution in the same fish, as given by Norris and Hughes (1920), are not unfavourable
to this interpretation of it. The nerve is, however, said by Norris and Hughes to arise
from ganglionic cells in the Gasserian ganglion, while the fibers of the ophthalmicus profundus
simply traverse that ganglion. The nerve, as I find and define it in Chlamydoselachus, is
large, and running forward dorsal to all the nerves and muscles of the orbit, traverses the
Text-figure 119.
Gangliated roots of fifth, seventh and eighth cranial nerves of Chlamy-
doselachus: A, lateral view; B, medial (inner) view.
Bucc., ramus buccalis VII; H., ganglion of the truncus hyomandibularis (ie., the true
ganglion of the facialis, combined with the acustico-lateralis ganglion); Man.V and Max.V,
mandibular and maxillary divisions of the facial nerve; P.L., pars intermedia; Pro., profundus
branch of the facial; R.C., ramus communicans; R.V., root of trigeminal nerve; S.Op.V
and S.Op.VII, superficial ophthalmic divisions of the fifth and seventh cranial nerves.
After Hawkes, 1906, Figs. 2 and 3, pl. LX VIII.
preorbital foramen and reaches the dorsal surface of the nasal capsule, where it immediately
breaks up into numerous branches which spread out, fan-shaped, and innervate the sensory
organs of the supraorbital laterosensory canal and the supraorbital ampullae, as shown in the
figures. As the nerve traverses the orbit a number of branches are sent upward through the
foramina supraorbitalia to the related portion of the supraorbital canal.
The- maxillary and the mandibular rami of the trigeminal nerve (Max. V. and
Man. V. in Text-figure 119) come off separately from the Gasserian ganglion; there is
no common maxillomandibular trunk. This condition is somewhat exceptional among
elasmobranchs. Since, in Chlamydoselachus, the angle of the jaw is situated far posteriorly,
the mandibular nerve leaves the maxillary early in its course and passes over the posterior
wall of the orbit to reach the angle of the mouth, as in Acanthias. The mandibular
nerve does not supply the large median transverse muscle bridging the halves of the lower
jaw in the gular region (Furbringer, 1903; Hawkes, 1906; Luther, 1909; Allis, 1917 and
This unique feature has been fully discussed (p. 399) in the section on the
muscular system.
a a il le
The Anatomy of Chlamydoselachus 481
Hawkes finds many small branches of the maxillary nerve which terminate in the
mucosa of the roof of the mouth and are therefore visceral, but she thinks it probable
that these visceral components belong to the facial nerve and are only secondarily united
with the trigeminal.
Every student of comparative anatomy is familiar with the difficulty of separating
the fifth and the seventh nerves where parts of different nerves are interwoven or run
in the same sheath. Hawkes (1906, pp. 968 and 969) states that in Chlamydoselachus:
No complete union between the [fifth and seventh] nerves has been found, except for
a distance of about 1 cm. on the left side, where a branch of the ramus buccalis and of the ramus
maxillaris are inseparable. The appearance of union occurs chiefly in the region just beyond
the orbit, where there are plexiform connections between the buccalis VII, mandibularis V,
maxillaris V, and their branches. Here, when two or more nerves come into close contact,
they are loosely or tightly bound together by connective tissue, but, in all cases except the
one mentioned above, in such a way that a separation can be effected by careful dissection.
The smaller branches and these pseudo-unions vary considerably on the two sides of the
same specimen and in different specimens. The variability, which is met with in every
system of Chlamydoselachus, suggests that the species has considerable anatomical instability.
There is considerable difference of opinion as to what parts, in the region of the
gangliated roots, belong to the fifth and seventh nerves respectively. In most elasmo-
branchs the ganglion of the buccal division of the seventh or facial nerve is intimately
associated with the Gasserian ganglion, and the two are often inseparable. In Chlamy-
doselachus the two ganglia are distinct medially, as shown in Text-figure 119s, after
Hawkes. Concerning some interrelations of the fifth and seventh nerves Allis (1923, pp.
209 and 210) writes:
The nervi profundus and trigeminus, as I interpret these nerves, arise by two main
roots, the anteroventral one of which is formed by the combined roots of the profundus
and that part of the trigeminus that is currently considered to form the entire nerve. The
other root arises by two rootlets, in close connection with the root of the nervus facialis, the
two rootlets being the facialis roots A and B of Merritt Hawkes’ descriptions. This root
joins the anteroventral root inside the cranial cavity, and, in the specimen used for the
accompanying Fig. 58, the two roots traverse the membrane that forms the mesial wall of
the acustico-trigemino-facialis recess through a single foramen which lies anterior to the
foramen for the root of the nervus facialis and wholly separate from it. In the acustico-
trigemino-facialis recess these two roots enter a ganglionic complex, but this complex was
not particularly examined. According to Merritt Hawkes a ganglion forms on each of the
two roots, one of which she calls the Gasserian ganglion and the other the buccalis ganglion,
the latter ganglion lying dorsal to the former and wholly [?] separate from it. On the “inner
side” of the Gasserian ganglion there is said to be a small swelling, from which the rami
profundus and superficial ophthalmic V arise, side by side and of equal size. Comparison
of these conditions, as thus described, with those in Squalus acanthias and Mustelus califor-
nicus, as described by Norris and Hughes (1920), would seem to establish beyond question that
the anterior root of Chlamydoselachus is composed entirely of motor and general sensory
(spinal V) fibers, that the little swelling on the inner side of the so-called Gasserian ganglion
is the ganglion of the nervus profundus, and that the posterior root of the complex derives
482 Bashford Dean Memorial Volume
its fibers both from the lateral line lobe and the acusticum. Whether these latter fibers are
all strictly laterosensory ones, as Norris and Hughes conclude, or are in part to be compared
to the communis fibers that enter into the trigeminus in the Teleostomi, seems to me still an
open question. The three fine nerve strands said by Merritt Hawkes to be sent from the
Gasserian ganglion to the facialis ganglion are evidently general sensory ones, as Merritt
Hawkes suggests.
In one respect, according to Hawkes (1906), the facial nerve is in an unusually
primitive condition, in that it has a remnant of the post-trematic ramus quite separate
from the truncus hyomandibularis. Hawkes states that a chorda tympani, as defined by
Cole (1896) and by Herrick (1899), is present; but Allis (1923) writes that the so-called
chorda tympani described by Hawkes seems to be a ramus pretrematicus internus and
hence, according to recent opinion, not the chorda. Further, the ramus mandibularis
internus passes internal to the ligamentum mandibulo-hyoideum and then forward along
the internal surface of the mandible, supplying the tissues of that region. This nerve,
according to Allis, isa ramus post-trematicus internus facialis and is the one now generally
considered to represent the chorda tympani.
Hawkes describes, in Chlamydoselachus, a small branch of the glossopharyngeal
nerve innervating neuromasts. A branch similar in function has been described in
Squalus acanthias by Norris and Hughes (1920), but they state that in Raja radiata
there are no lateral line elements in the ninth nerve.
Brohmer (1909) finds, between the facialis acusticus and the glossopharyngeal
nerves of his 25-mm. embryo, a small ventral root (Text-figure 118, Gl.v.) which he inter-
prets as belonging to the glossopharyngeal. He thinks it likely that this ventral root
disappears in later stages, and names it “the rudimentary ventral root of the glosso-
pharyngeal nerve.” Goodrich (1918.2) represents (by a dotted line in front of gl.) this
root in his schematic Text-fig. 1, reproduced as Text-figure 117 herein.
Garman (1885.2) states that in his specimen “The tenth pair (vagus) is somewhat
asymmetrical, having eight roots on one side and twelve on the other. There are also
four pairs of ventral roots near the median line.” Hawkes (1906) states that the vagus
arises by from nine to twelve roots from the hinder end of the medulla. The lateralis
root, which is the most cephalad, is invariably large, the remainder are small. These
small roots are not symmetrical in number and arrangement even in the same fish, much
less do they agree in different fishes. The roots arise at the same level, being arranged in
an arc which extends along the side of the medulla to the beginning of the spinal cord.
The roots cannot be assigned to the separate rami, and the ganglia of the vagus cannot
be separated completely by gross methods. The ramus lateralis vagi unites closely with
the true vagus in the ganglionic region. There is a sixth ramus branchialis vagi which
passes toward the remnants of the seventh branchial arch. Hawkes found no trace of
any median ventral roots uniting with the vagal complex. Commenting on Garman’s
statement concerning the presence of ventral roots in his specimen, Hawkes writes:
“If Garman were right, his specimen suggests the retention of the somatic motor compo-
The Anatomy of Chlamydoselachus 483
nent of the vagus, whereas, in all cases, so far as is known, the remains of that component
have passed [as ventral occipitospinal roots] into the hypoglossal. ... This would indeed
be a primitive condition.” Garman (1885.2) does not mention any occipitospinal nerves,
but the ventral roots labeled ‘‘10” in his Fig. A, pl. XVI (my Figure 26, plate VI) are
probably occipitospinales.
Hawkes found, in Chlamydoselachus, four (pairs?) of spino-occipital (occipitospinal)
nerves, which pass out of the cranium by four separate foramina. Three of these roots
are shown in Figure 13, plate IV, after Hawkes. No ventral occipitospinal roots
are shown in Hawkes’ figure of the ventral surface of the brain. She records that two of
the occipitospinal roots were placed completely under, the third partly under, the cover
of the vagal roots. Immediately outside the cranium the occipitospinal nerves unite into
a flattened strand, the hypoglossal nerve. Hawkes states that the third and fourth
occipitospinales of Chlamydoselachus have each a dorsal branch, which, like the dorsal
branches of the succeeding spinal nerves, passes upward and backward. No dorsal
branches were found on the first two occipitospinal nerves.
Johnston (1905.1, p. 231) interprets the occipitospinal nerves as follows: “The
dorsal and ventral ‘hypoglossal’ roots need not be considered as spinalartige nerves.
They probably are not equivalent to spinal nerves at all, but are only the general cutaneous
and somatic motor components of nerves of the vagus region, the visceral sensory and
motor components of which have been collected into a single large vagus root.”
In his 25-mm. embryo, Brohmer (1909) describes and figures (my Text-figure 118)
a series of ventral roots lying between the main branches of the vagus. The first of these
(1.v.) is present on only one side, and is very small; the others are paired. Brohmer
states that six of these ventral roots are occipitospinal nerves, but it seems possible
that only four or five of the most anterior ones are really occipitospinales, the remaining
posterior ones being ventral roots of spinal nerves. (Daniel, 1934, states that “as many
as five” of the ventral occipitospinales have been located on each side in the young of
Heptanchus and Chlamydoselachus). Dorsal to the third and fourth ventral roots,
Brohmer found two ganglionic masses (Ggl.1., Ggl.2.), which he interprets as remains
of the ganglionic crest. The more posterior of the two masses has two rootlets.
In Heptanchus (Furbringer, 1897; Daniel, 1934) there are four pairs of ventral
occipitospinal nerves or roots (Text-figure 116, w-z), but only two pairs of dorsal roots
(Figure 28, plate VII). The members of the first dorsal pair join the corresponding
members of the third ventral pair to form a pair of nerve trunks resembling spinal nerves
in that they have both dorsal and ventral roots. The first roots to arise ventrally are
near the median line and in origin are not unlike the sixth or abducens nerves.
In a 26mm. embryo of Spinax described by Braus (1899) there were four pairs of
ventral roots representing occipitospinal nerves. Of these, one on the left and two on
the right were joined by dorsal roots bearing ganglia, thus increasing the resemblance
to spinal nerves.
484 Bashford Dean Memorial Volume
The number of occipitospinal roots in Chlamydoselachus, Heptanchus and Spinax
is unusually large. In Squalus (Text-figure 120) there are only two or three ventral
and two dorsal occipitospinal roots. These nerves united with the first and second
spinals are marked hb. in the figure. In Torpedo, a single (ventral) occipitospinal root
is present (Daniel, 1934).
According to Daniel (1934), the occipitospinal nerves of Heptanchus innervate the
subspinalis and dorsal interarcuales muscles; also, in elasmobranchs generally, the more
posterior of these nerves unite with the first group of spinal nerves to form the cervical
Text-figure 120.
A projection, upon a sagittal plane, of the cranial, occipital and anterior spinal nerves of Squalus acanthias.
br.p., brachial plexus; bu. VII, buccalis of seventh nerve; d.X, ramus dorsalis of tenth; gn., first spinal ganglion; hb., hypobranchial
bundle; hmd., hyomandibularis; I].X, lateral line nerve; md.e. VII, mandibularis externus of seventh; md.i.VII, mandibularis internus
of seventh; md.V, mandibularis of fifth; mx.V, maxillaris of fifth; op.V, ophthalmicus profundus; os.V, and os. VII, ophthalmicus
superficialis of fifth and seventh; ph.IX, pharyngeal branch of ninth; pl. VII, palatinus of seventh; po.t., post-trematicus of ninth;
pr.t., pretrematicus of ninth; sp., spiracle; st.1X, supratemporalis of ninth; st.X, supratemporalis of tenth; vi.X, visceral nerve; y and z,
occipitospinal nerves; II, optic; III, oculomotor; IV, trochlearis; VI, abducens; VIII, auditory nerve.
From Daniel, 1934, Fig. 220; after Norris and Hughes, 1920, fig. 51 (in colors).
plexus which in turn joins the pectoral plexus. The nerves of the cervical plexus separate
from the pectoral plexus and pass in front of the girdle to supply the hypobranchial
muscles, as in Scyllium and in Squatina (Furbringer, 1897).
In her summary for the cranial nerves, Hawkes (1906) notes that the lower jaw of
Chlamydoselachus has been swung far back into a reptilian position, and suggests that
this may explain: (a) the absence of a typical maxillo-mandibular trunk; (b) the union of
branches of the vagus with one another and with the ramus lateralis vagi; and (c) the
great development of a hypoglossal musculature and the presence of a hypoglossal nerve.
She states that the number of roots by which the lateralis components arise confirms the
suggestion that, in origin, the acustico-lateralis components belong to a series of segments.
The connections between the acustico-lateralis elements of V, VII, and VIII show a ten-
The Anatomy of Chlamydoselachus 485
dency toward unification of the system. The trigemino-facial complex is less primitive
than that of Chimaera, but more so than that of most elasmobranchs. Hawkes’ general
conclusion is that the cranial nerves of Chlamydoselachus are not in so primitive a con-
dition as would be expected from the low position of the species in the taxonomic series,
especially as regards the vagus and the lateralis nerves.
THE SPINAL NERVES
Hawkes’ description (1906, pp. 985-987) of the spinal nerves of Chlamydoselachus
is concerned mainly with the spinal nerve roots. I quote her account almost entire:
The ventral root of the first true or complete spinal nerve originates between the first
and second vertebrae. Spinal nerves 1, 2, 3, 4, 5 (Fig. 1, pl. LXVIII) [my Figure 29, plate
VII] unite with the spino-occipital nerves into a strand, which passes backwards, then out-
Text-figure 121.
Diagram of spinal nerves from anterior, middle
and tail regions of Chlamydoselachus.
C.S., connecting strands between dorsal and ventral roots;
D.B., dorsal branch; D.R.G., dorsal root with its ganglion;
No., notochord; S.N., spinal nerve; V.B., ventral branch;
V. C., vertebral column; V. R., ventral root.
After Hawkes, 1906, Text-fig. 141.
wards towards the pectoral girdle. Spinal nerves 6 and 7 unite with one another before
joining this plexus. Spinal nerve 8 runs by its side, but does not actually join. The spinal
plexus gives off anteriorly two branches (S.h.1 and S.h.2). Branch S.h.1, which is connected
with vagus 6, passes forwards and downwards to join branch S.h.2. The resulting compound
nerve passes forward near the median ventral line to supply a portion of the median man-
dibular or hypoglossal musculature. It is probable that this nerve consists only of fibers from
the spino-occipital nerves, and would therefore be the homologue of the hypoglossal nerve
of higher forms.
The brachial plexus consists of the remaining parts of the composite strand, i.e., the
first eight complete spinal nerves of which the last remains distinct. The brachial plexus is
here in a simple condition, for it consists of but few nerves, and those are not intimately
united. ...
Each spinal nerve arises by two alternate roots, a dorsal anda ventral. The ventral root
[V.R.] arises by three rootlets, then, after emerging from the vertebral column, gives off
a large dorsal branch (Text-fig. 141, D.B.) [my Text-figure 121] before uniting with the dorsal,
ganglionated root [D.R.G.]. In the anterior and middle regions of the vertebral column,
this union takes place at a level with the top of the notochord, but in the tail region at a level
with the base of the notochord, immediately to the inner side of the ramus lateralis vagi.
The ventral branch (V.B.) is given off at varying points (Text-fig. 141) [my Text-figure 121].
The dorsal branch (D.B.) of the ventral root runs caudad and upwards, passing over
the ganglion of the dorsal root (D.R.G.) to be distributed to the muscles of the middle region of
the back. A similar root (ventral-dorsal) has been described by Ewart and Cole in Raia. No
dorsal branch was found for the complete spinal nerve or for the dorsal root, as it is probable
that the dorsal branch of the ventral root receives fibres from the dorsal root as it passes
over the latter on its backward course. In one segment (Text-fig. 141) [my Text-figure 121]
486 Bashford Dean Memorial Volume
Text-figure 122.
Nervus collector, consisting of longitudinal strands connecting the ventral rami of certain
of the spinal nerves, in Chlamydoselachus.
I.a.v., lateral abdominal vein; pl.p., pelvic plexus; sp.25,38, twenty-fifth and thirty-eight spinal nerves.
From Daniel, 1934, Fig. 224; after Braus, 1898, Fig. 1, Taf. XIII.
the dorsal branch of the ventral root could be seen, by the naked eye, running over the
dorsal root ganglion, from which it could not be separated; in the succeeding segment the
dorsal and ventral roots were joined in the region of the sensory ganglion, and the dorsal
branch appeared to arise from the ganglion itself. The spinal nerves here recall the condition
of Laemargus, of Bdellostoma, and of Myxine, in that all three have (1) several rootlets for
the ventral root, (2) a dorsal branch from the ventral root which unites with the dorsal
root ganglion or with some portion of the dorsal root.
The “‘nervus collector” studied by Braus (1898) in Chlamydoselachus and in a number
of other elasmobranchs, consists of one or more longitudinal strands connecting the ventral
rami of some of the spinal nerves situated posterior to the pectoral fin and in the region
of the lateral abdominal vein. The principal collector nerve of Chlamydoselachus (Text-
figure 122) is plexiform, and consists of a multitude of anastomosing strands together with
some branches that end freely. The nervus collector, though variable, appears to be
best developed in primitive forms like Chlamydoselachus and Heptanchus (Text-figure
123), in both of which the twenty-fifth to the thirty-eight spinal nerves take part. The
sp.25
Text-figure 123.
Nervus collector, connecting the ventral rami of certain of the spinal nerves, in Heptanchus cinereus.
1.a., lateral artery; |.a.v., lateral abdominal vein; pl.p., pelvic plexus; sp. 25,38, twenty-fifth and thirty-eighth spinal nerves,
From Daniel, 1934, Fig. 205; after Braus, 1898, Fig. 1, Taf. XI.
The Anatomy of Chlamydoselachus 487
collector is much more complex in Chlamydoselachus than it is in Heptanchus. In other
forms few nerves take part (as in Spinax), or the collector may be absent (as in Squatina
and in Raja).
The nervus collector has been studied minutely by Braus and others (cited by
Osburn, 1906 and 1907) because of its possible relation to the origin of the paired fins,
with results that have been interpreted differently by exponents of the gillarch and
fin-fold theories respectively.
From a functional point of view, the nervus collector is somewhat comparable to
the caudal longitudinal collecting nerve trunks described by Speidel (1923) in Squalus
acanthias and in Raja laevis. In both cases, the longitudinal trunks and accompanying
nervous network provide a conducting system which may be effective in the coordi-
nation of muscular action.
The innervation of the tropeic folds, described by Braus (1898), has been considered
in the section on the muscular system and is illustrated by my Text-figure 59, p. 386.
THE SENSE ORGANS
This account of the sense organs of Chlamydoselachus is necessarily very incomplete.
None of these organs has been described histologically, and my material is unfit for
study in serial sections.
The external openings of the olfactory sacs have been described by Gudger and
Smith (1933), whose account is based on the descriptions of various authors, supple-
mented by their own observations; but the internal structure of the olfactory organs of
Chlamydoselachus has never been described.
The external appearance of the eye and the peculiar mechanism by which the
cornea may be protected in the absence of lids have been described by Gudger and Smith
(1933). In the present paper I have described the muscles of the eye and their innervation,
in the sections on the muscular system and the nervous system respectively. The internal
structure of the eye has never been described.
Of the various sense organs of Chlamydoselachus, the lateral line or sensory canal
system and associated organs have received the most attention, but even here the various
authors (Garman, 1888; Hawkes, 1906; and Allis, 1923) are concerned only with gross
structure and distribution. The ear (membranous labyrinth) has been studied and describ-
ed by Goodey (1910.1).
THE MEMBRANOUS LABYRINTH
Goodey’s (1910.1) Figs. 7 and 8, pl. XLIII, illustrating medial and lateral views of
the membranous labyrinth of Chlamydoselachus, are reproduced as my Figures 30 and 31,
Plate VII. His description (pp. 551 and 552) of this organ is best given in his own words:
On removing the skin from the dorsal surface of the cranium it is seen that the parietal
fossa is rather deep and possesses four apertures, two on either side of the median longitudinal
line. One of these apertures, the anterior, is small, and transmits the ductus endolymphaticus.
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Bashford Dean Memorial Volume
The posterior is larger and is closed with soft subcutaneous tissue. It is an opening into
the perilymph cavity surrounding the posterior vertical canal, and seems to correspond to
the tympanic aperture which Howes (1883) described in Raia. Before proceeding further,
I may mention that in this account I am following the nomenclature used by Stewart (1906),
which differs somewhat from that used by Retzius (1881) in his great monograph.
The ductus endolymphaticus, on emerging from its cranial foramen, soon expands
into the saccus endolymphaticus. The latter lies partly in the parietal fossa and is partly
attached to the under surface of the skin covering this region. It is fairly regular in shape,
somewhat rounded on its anterior surface, and extends posteriorly in a slightly outward
direction, gradually becoming attenuated until it reaches its external aperture, which is
quite small. Internally the ductus endolymphaticus leads into the sacculus. This is not
rounded, but is laterally flattened, and gives off at its postero-inferior end the lagena in the
form of a simple caecum.
The utriculus in this species is like that in other Elasmobranchs, being divided into
two portions, anterior and posterior, which do not communicate directly with each other,
but indirectly through the sacculus.
The anterior utricle is rather laterally compressed and gives off the anterior canal
dorsally. The latter curves forward and slightly outward, and describes almost a semicircle
in its course, expanding at its lower end into the anterior ampulla, which then opens by
a wide portion into the lower end of the utricle again.
The recessus utriculi is a somewhat spherical structure on the inferior and outer border
of the anterior utricle. It communicates with the latter by means of a slit-like aperture just
below that leading into the ampulla externus. The anterior utricle does not open directly
into the sacculus, but communicates indirectly with it through the recessus utriculi, which
opens into the sacculus by means of a rounded aperture on the posterodorsal side of the
recessus.
Arising from the dorsal end of the anterior utricle, and proceeding in a posterior and
outward direction, is the external canal, which bends downward and comes to lie in an
almost horizontal position. At its anterior end it is slightly elevated and expands into the
ampulla externus, which communicates with the anterior utricle again by means of a short
canal which rests on the upper side of the recessus utriculi, but does not open directly into it.
The posterior utricle, which is situated more internally than the rest of the labyrinth, is
somewhat cylindrical in shape and is slightly curved upon itself. It communicates directly
with the sacculus by means of a short, almost vertical canal, the ductus utriculo-saccularis
posterior. Arising from its dorsal end is the posterior canal, which curves outward and
downward, and then expands into the posterior ampulla, which opens into the lower end of the
utricle again.
All three canals, anterior and posterior vertical, and external horizontal, are not rounded
in section, but are markedly flattened, so that their height is equal to about twice their width.
The external canal in its almost horizontal position lies with its compressed sides in the
horizontal plane.
Goodey then continues with an account of the nerve supply of the membranous
labyrinth. In conclusion, he states that in structure and in the distribution of the nerve
supply the membranous labyrinth of Chlamydoselachus resembles rather closely that of
Notidanus (Hexanchus) griseus figured by Stewart, 1906. The membranous labyrinth
of Heptanchus is described and figured by Daniel (1934).
The Anatomy of Chlamydoselachus 489
THE SENSORY CANAL SYSTEM
The distribution of the sensory canals of Chlamydoselachus has been described by
Garman (1888), Hawkes (1906) and Allis (1923 and 1934). Their descriptions have been
briefly reviewed by Gudger and Smith (1933), who added some observations on the
specimens in the American Museum of
Natural History. This account, which is
fairly well illustrated, need not be repeated
here. Some of the sensory canals of the
head are shown in my Text-figure 70,
page 396; and in Text-figure 124. The
innervation of the sensory canals of the
head has been worked out by Hawkes
(1906), whose drawing is reproduced as
my Figure 29, plate VII. For comparison,
I have inserted a similar figure (Text-figure
125) representing the sensory canals of
the head in Squalus. It remains to con-
sider the sensory canal system of Chlamy-
doselachus briefly from a comparative
point of view.
In all adult elasmobranchs, the sen-
sory canals are fairly similar in their dis-
tribution. A pair of these canals extend
in or under the skin, from the tip of the
tail to the vicinity of the ear, where they
connect with other canals branching over
the various regions of the head. At inter-
vals, the canals open to the exterior by
means of pores, so that their approximate
distribution can usually be traced without
dissection.
Among living elasmobranchs it is
very unusual for the sensory canals to be
present as open grooves through so great
a portion of their extent as is the case in
Text-figure 124.
Dorsal view of the head of Chlamydoselachus, show-
ing the external openings of the ampullae of Lorenzini
and of the laterosensory canals.
amp, ampullary pores; end, pore of the endolymphatic duct; iop,
infraorbital laterosensory pores; llc, lateral line canal of body;
sop, supraorbital laterosensory pores; sp, spiracular laterosensory
canal; spr, spiracle.
Redrawn after Allis, 1923, Pl. II.
Chlamydoselachus. The lateral line of Chlamydoselachus is an open groove from the tip of
the tail almost as far forward as the spiracle (Garman, 1888). The anterior portion of the
lateral line (IIc.) is shown in Text-figure 124. Several of the longest sensory canals of the
head are open—in particular, the spiracular (sp. in Text-figure 124), the gular and the oral.
The latter are shown in Gudger and Smith’s (1933) Figure 7, plate II, after Allis; they
appear, without labels, in my Text-figure 70, page 396. In Figure 29, plate VII, after
490 Bashford Dean Memorial Volume
Text-figure 125.
Innervation of the sensory canal system and certain of the pit organs in Squalus acanthias.
bu. VII, buccalis nerve; cc., supratemporal canal; dr.X, ramus dorsalis of tenth nerve; hmc., hyomandibular
canal; ioc., infraorbital canal; JI., lateral line canal; JI.X, lateral line nerve; me., mandibular canal: mde. VII,
external mandibular nerve; os. VII, ophthalmicus superficialis of seventh nerve; po., pit organs; soc., supraorbital
canal; st.IX, supratemporalis of ninth nerve; st.X, supratemporalis of tenth nerve.
From Daniel, 1934, Fig. 245; after Norris and Hughes, 1920, Fig. 50.
Hawkes, the oral, gular and spiracular are labeled HLA, HLB and HLC respectively.
The preceding statements concerning the open condition of the canals hold for my four
large specimens, save that on the right side of No. I the groove is lacking for a distance
of about 30 mm. from the tip of the tail.
A more extensive occurrence of sensory canals as open grooves is found in the
Holocephali, where most of the canals, including those of the head, are open; but in the
Selachii, Chlamydoselachus appears to be unique in the extent to which its sensory canals
are open. The nearest approach to its condition in this respect is found in the notidanids
(Daniel, 1934), where the lateral line is an open groove as far forward as the pectoral fin.
In Heptanchus the canals of the head are all closed tubes, as far back as the fifth gill-cleft.
Posterior to this, the lateral lines are represented by a pair of open grooves extending
almost to the tip of the tail. In Squalus (Text-figure 125) the canals are closed excepting
in the region toward the tip of the tail. In higher elasmobranchs, the canals are usually
closed throughout their entire length.
The open condition of the sensory canals found by Garman in Chlamydoselachus
(Text-figure 126) is probably primitive, and in the light of all the evidence can scarcely
be explained as due to arrested development in the embryonic sense. Lateral line canals
as Open grooves were found by Dean (1909, p. 252) in the Devonian fossil shark Ctenacan-
thus clarkii (Text-figure 127) as well as in many acanthodians. In all these forms the
dermal denticles terminate abruptly at the margins of the groove, and the marginal
denticles are, in most instances, unusually large, precisely as they are in Chlamydoselachus.
Most of the terms used by Garman in describing the sensory canals of the head in
his specimen have been abandoned, and in their places are names for the various divisions
The Anatomy of Chlamydoselachus
based on their innervation. Concerning
certain sensory canals of Chlamydoselachus
Garman (1888, pp. 82 and 83) writes:
The aural [supratemporal ] canal is closed.
It has no tubules. Contrary to what obtains
in other Galei, it lies in front of the so-called
ear openings [endolymphatic ducts]. These
openings, however, are at the ends of tubes the
inner extremities of which are in front of the
[supratemporal] canal. The canal is nearly
straight, bending slightly forward in the middle
and a little backward near each end. ... At
the end of the jugular, near the middle of the
first branchial aperture, there are two branches
not found in any other of the sharks examined:
a spiracular [HLC in Figure 29, plate VII],
turning upward and forward toward the spir-
acle; and a gular [HLB in Figure 29, plate
VII], turning down and forward near the
median line, and finally uniting with the oral
[HLA in Figure 29, plate VII] a short distance
from the inner end. . . . Apparently the pre-
nasal is reversed in direction, meeting the nasal
in front and running backward to join the sub-
rostral. . . . Like the corporals, the oral, gular
Text-figure 128.
Variations in lateral line canals of Chlamydo-
selachus: A and B, supratemporal or commissural
canal; C and D, ventral view of hyomandibular
canal under the lower jaw; E, lateral line canal
in the region of the dorsal fin.
C.C.A. and C.C.B., anterior and posterior portions of com-
missural canal; H.M., parts of the hyomandibular canal;
L.L.R. and L.L.L., lateral canal on right and left sides.
S., vestigial canals (?).
After Hawkes, 1906, Text-fig. 140.
Text-figure 126.
Portions of open lateral line canals in a living and
in an extinct shark.
Text-figure 127.
Textfigure 126. The open lateral line canal in
the tail region of Chlamydoselachus. Note the
elongate scales (x 5) which partially cover the
open canal.
After Garman, 1885.2, Fig. 10, pl. VI. ;
Text-figure 127. Lateral line canal of the fossil
shark Ctenacanthus clarki, showing the enlarged
denticles at the margin of the groove.
After Dean, 1909, Fig. 44.
and spiracular [canals] are open grooves.
In the spiraculars and gulars of this shark
are found the nearest approach to the pleu-
rals of the Batoidei.
Hawkes (1906) states that the lateral
line system of the head of Chlamydosela-
chus is much more complicated than is
usual among elasmobranchs (excepting rays
and skates). Evidently, she refers merely
to the gross pattern or topographical
relations of these canals. The supratem-
poral or commissural canal in Chlamydo-
selachus is placed anterior to the openings
of the ductus endolymphaticus, and is
never the usual straight, transverse line
connecting the right and left lateral canals.
It varies greatly, as shown in her Text-fig.
140 (my Text-figure 128a ands). There
are indications of two instead of one com-
492 Bashford Dean Memorial Volume
missural canal, but it is impossible to state whether the present condition of these canals
is vestigial or rudimentary. It is certain, however, that the condition of all the canals,
but especially those in this region, is very unstable. Some variations in the hyomandibular
region are shown in Text-figure 128c and p; other variations, in the pelvic and caudal
portions of the lateral line, are represented in Text-figure 128z. Additional examples of
variation in the posterior course of the lateral line are described by Gudger and Smith
(1933, pp. 288-9) in three adult specimens.
Hawkes concludes that the lateral line system of Chlamydoselachus is primitive as
regards: (1) the open condition of a portion of the canals; (2) the cutaneous rather than
subcutaneous position of the canals; and (3) the entire absence of tubules in many places.
In the occipital and hyomandibular region, however, the system tends to a considerable
topographical complexity. Again there are indications, in the occipital and lateral canals,
of either a vestigial or a rudimentary complexity.
In Heptanchus (Daniel, 1934), anterior to the spiracle and just posterior to the
endolymphatic duct, a small transverse or supratemporal canal passes off from the lateral
canal toward the median line. This, however, does not meet and fuse with the similar ca-
nal from the opposite side. In Heptanchus maculatus there may be two supratemporal
canals on a side, one posterior to the endolymphatic duct, the other anterior to it. Thus
we find evidence, in this region, of a variability somewhat comparable to that described
in Chlamydoselachus. In Heptanchus, Daniel describes a “‘gular line” of pit organs corre-
sponding in position to Garman’s gular division of the sensory canal system in Chlamy-
doselachus. Allis (1923; 1934), like Garman, describes and figures the gular line as a part
of the canal system. “The spiracular and gular canals [of Chlamydoselachus] form
a continuous open groove” (Allis, 1923). This statement holds, without exception, for
both right and left sides of my four large specimens. Norris (1929) writes: ‘The
mandibular series of pit organs in Squalus (Norris and Hughes, 1920) and Mustelus
(Johnson, 1917) evidently correspond to the gular canal organs in Chlamydoselachus
(Hawkes, Allis)”.
Many other comparisons of the sensory canal, ampullary and pit organs of Chlamy-
doselachus with those of other elasmobranchs are elaborated in the works of some of the
authors cited, but these involve details that cannot be considered here.
DISCUSSION
The present section is concerned with the phylogenetic significance of the anatomical
characters described on the preceding pages. In every section of this article, comparisons
have been made between Chlamydoselachus and other vertebrates, so that it is not neces-
sary to enter into details here.
My own interest in Chlamydoselachus relates chiefly to the evolution of organs and
organ systems as such. Nevertheless, while studying this shark I have been impressed
by certain things that have a bearing on the question of its phylogenetic affinities: first,
The Anatomy of Chlamydoselachus 493
in some features it seems more primitive than any other living shark; second, in certain
other respects it is highly specialized; third, it possesses some characters that are unique;
fourth, it combines (as in the spiral intestine) some characters that are ordinarily segre-
gated in different species; and fifth, it is highly variable. Within obvious limits, the
frilled shark is a comprehensive type, and this constitutes one of the difficulties in the
way of determining its afhinities.
It is recognized that we are here on treacherous ground. Opinions will differ con-
cerning the evaluation of the anatomical characters of Chlamydoselachus, and concerning
the status of the animal as a whole. Nevertheless, to give point to the discussion I have
summarized the most important data (Tables IV and V, pp. 496-497) in two lists of
characters: one palingenetic or primitive, the other cenogenetic or of relatively recent
origin, with reference to comparable structures in other living sharks. Some very obvious
features, such as the unusual number of gill-slits and the dorsoventral flattening of the
head, are excluded because of insufficient evidence as to their status. It is not expected
that anyone will accept either list in its entirety. Each list might be greatly extended,
affording endless opportunities for debate.
The more striking peculiarities of Chlamydoselachus, such as the very elongate
form of the body and the peculiar hyostylism of the skull, are obviously cenogenetic.
The real difficulty lies in the disguises which may conceal other cenogenetic characters.
Apparent primitiveness is frequently the result of degeneration or retrogession, in
a phylogenetic sense; this, as applied to the individual, is usually a matter of arrested
development. In Chlamydoselachus there are evidences of retrogression in the skeletons
of the fins, in the mesonephric duct and urinary sinus of the right side, and in the vestigial
seventh gillarch. In each case there are decided irregularities. It seems to be a fairly
general rule that, when the development of an organ is arrested, it does not merely fail
to attain the ancestral condition, but exhibits a vestigial complexity.
In Chlamydoselachus there are features, such as the thin walls and large foramina
of the cranium, the incipient cyclospondylous vertebral centra, and the paired condition
of the urinary sinuses in the adult, that appear more characteristic of an immature than of
an adult shark. The position of the epibranchial arteries is that found in the embryos
of other sharks. In all these cases there is no evidence that development has ever gone
further. The alternative is to accept these features as primitive characters. The per-
sistent thyroglossal duct may be anomalous, since it is not found in all specimens. Since
the so-called duct differentiates like the wall of the pharynx, from which it is derived,
it is obviously something more than an embryonic rudiment.
I have said that, within obvious limits, Chlamydoselachus is a comprehensive type.
This is true mainly with respect to features that may be found in other sharks, but some
of the resemblances to higher vertebrates are striking. Of these, it is sufficient to mention
the extreme length and mobility of the jaws, suggestive of the Ophidia; the gular fold,
simulating a condition found in many of the Teleostomi; and the armature of scales on
494 Bashford Dean Memorial Volume
the anterior border of the dorsal fin, resembling in form and arrangement the “‘fulcral
scales” of the Actinopterygii. It is scarcely necessary to add that these resemblances to
higher vertebrates have no phylogenetic significance.
The expression “oldest living type of vertebrate” used by Garman (1884.3 and
1884.4) and by Gill (1884.1 and 1884.2) with reference to Chlamydoselachus, quite ignores
the cyclostomes. While the cyclostomes are in some respects degenerate, in others
highly organized, they retain, to a greater degree than any other vertebrates, the funda-
mental chordate structures. The view that skeletal degeneration has been a major trend
in fish history has its limitations, particularly when one considers the endoskeleton rather
than the external armor. Cartilaginous, calcified and bony vertebral centra develop
largely at the expense of the notochord, and it seems unlikely that degeneration of the
harder structures would result in the notochord being restored to its primitive condition
as an effective organ in the adult. In Cyclostomata, as in Holocephali, the notochord is
unimpaired. The ammocoetes larva of the lamprey links this form with the lower chor-
dates rather than with the fishes. If phylogeny be defined as the succession of adult
forms in the line of evolution, this latter evidence is not admissible, but if organisms are
genetically related in the adult stage, then they must be related at all stages of their
development. The cyclostomes have long been regarded as the lowest group of living
vertebrates (craniates), and the evidence in support of this view should not be lightly
set aside.
The very interesting question of the relationship of Chlamydoselachus to fossil
forms is one that Iam quite willing to leave to paleontologists. Such studies must remain
under the handicap that, in fossils, little knowledge is available concerning organs that
are quite as important as the more enduring skeleton. Since the “hard parts” of Chlamy-
doselachus, upon which we must depend for comparison with fossils, have long been
known, it can scarcely be expected that the present paper will add much that will be
of value to paleontologists. What has been added concerning the “soft parts” serves
to confirm the generally accepted systematic relationship of Chlamydoselachus to the
notidanids without, however, bringing them any nearer together. While Chlamydo-
selachus and the notidanids must be assigned to different families, the relationship is
closer than that between Chlamydoselachus and any other existing sharks. In this con-
nection the following quotation from Woodward (1921) seems pertinent:
The Hybodonts, which for the most part exhibit the primitive notochordal condition
until the Lower Cretaceous Period, are especially interesting because, while their dentition
and their general appearance resemble those of the existing Cestraciontidae, their skull is
very different and more closely agrees with that of the Notidanidae. They are indeed a
generalized group from which several later families appear to have arisen, and they are the
dominant sharks of the Jurassic and early Cretaceous periods.
Previous discussions of the affinities of the frilled shark to fossil forms have been
reviewed at length by Gudger and Smith (1933). Garman (1885.2) was particularly
impressed by the resemblance of the teeth of Chlamydoselachus (Text-figure 7, p. 344)
The Anatomy of Chlamydoselachus 495
to those of Cladodus, and went so far as to say that ‘““Chlamydoselachus is a cladodont.”
In the present paper (p. 349) I have compared the teeth of the frilled shark with those of
two cladodonts, Cladoselache and Cladodus, and two hybodonts, Ctenacanthus and
Hybodus (Text-figures 17, 18, 19, 20, on p. 348). The resemblance between the teeth of
Chlamydoselachus and the cladodonts is indeed striking, but the paleontological history
of Chlamydoselachus goes back no further than the Tertiary, while the cladodonts are
generally considered to be extinct since the Carboniferous. The teeth of hybodonts are
more generalized and variable; nevertheless, out of such structures, teeth like those of
Chlamydoselachus might readily have been evolved. The presence, in the hybodonts,
of a large spine at the anterior border of each dorsal fin does not exclude this family from
relationship with the Chlamydoselachidae. In the Spinacidae, some genera possess
spines similarly located, while other genera lack them.
Throughout this article I have recorded and emphasized the great variability of
Chlamydoselachus in most of its structures. The significance of this variability is not
self-evident. “As a paleontologist knows . . . variability is a special characteristic of
the struggling end of a disappearing race quite as frequently as it is a mark of the begin-
ning of a new race” (Woodward, 1933). There are reasons why, in the case of Chlamy-
doselachus, one may favor the former interpretation. The frilled shark has been taken
only in Japanese waters and off the western coast of Europe. If it were a new species,
one would not expect it to occur in waters so widely separated, particularly since it is
not gifted with extraordinary powers of locomotion. Since it is quite rare even in these
restricted localities, it seems to have a precarious hold on existence. It may be significant,
in this connection, that Chlamydoselachus anguineus is somewhat isolated in its systematic
position. The genus stands far enough from the Notidanidae to be placed in a separate
family, the Chlamydoselachidae, containing no other genera. There are no other species
save the fossil C. lawleyi and C. tobleri, both known only by their teeth (Text-figures
15 and 16, p. 348), and one may question whether the latter really belongs to the genus
Chlamydoselachus. The frilled shark appears to be a form that has long been differenti-
ated in adaptation for a particular habitat and mode of life, in which it has not been
altogether successful since it now seems to be facing extinction.
My outstanding impression of the frilled shark is that it presents a strange assem-
blage of characters ranging from very primitive to highly differentiated. In this, it is
comparable to Chimaera, though the latter is specialized in a decidedly different way.
Chlamydoselachus is a deep-sea adaptation of some rather ancient type of shark, and is
now waging a losing battle in the struggle for existence.’
'Since writing these pages I have found in Deinega’s (1925) English abstract of his Russian text the following statement: “We
may still consider Chlamydoselachus as one of the most ancient representatives of the vertebrates, having survived to our day and now
undergoing extinction” (italics mine). I do not know of any other author who has expressed the view that Chlamydoselachus is threaten-
ed with extinction. In my opinion, Chlamydoselachus is not “one of the most ancient representatives of the vertebrates.” It is,
however, one of the most primitive of existing sharks,
496 Bashford Dean Memorial Volume
TABLE IV.
PALINGENETIC CHARACTERS OF CHLAMYDOSELACHUS
Teeth, of “‘cladodont” type, are formed by the fusion of simple denticles.
At the angles of the mouth, scales grade into teeth.
The notochord persists with very little constriction.
Calcification of the endoskeleton is very limited in amount.
Cyclospondylous vertebral centra are incipient or rudimentary.
The visceral skeleton shows a striking gradation between jaws and gill-arches.
Nearly complete series of basibranchials and hypobranchials, with little fusion.
In the trunk musculature, longitudinal divisions are few and simple.
The digestive tube is relatively simple and is nearly straight.
The bursa entiana is not invaded by the spiral intestine.
In the valvular intestine, the apices of the anterior and posterior coils point in different directions.
In the middle portion of the spiral intestine, there is an axial strand; in both anterior and posterior portions,
there is an axial tube.
The liver is bilaterally symmetrical.
In some specimens, there is a persistent thyroglossal duct lined with pharyngeal mucosa.
Pouch-like vestige of the ventral end of the spiracular gill cleft.
In the female, the mesonephroi persist through almost the entire length of the body cavity.
In females, there is a pair of urinary sinuses which open separately into the urogenital sinus.
In females, nearly all the collecting tubules enter the mesonephric duct. So-called ureters are absent.
Epibranchial (efferent branchial) arteries are situated dorsal to the respective gill-arches, as in the embryos
of other sharks.
Posterior efferent collector arteries may retain a dorsal connection with the anterior efferent collector of the
same gill.
The brain is very small; the forebrain is small proportionally.
The roof of the definitive forebrain is said to be non-nervous.
Ina 25-mm. embryo, the glossopharyngeal nerve has a ventral root.
The “nervus collector” is unusually well developed.
The lateral line sensory canal is an open groove from the tip of the tail as far forward as the spiracle. Several
of the longer sensory canals of the head are open.
Whether open or closed, the sensory canals of the lateral line system are cutaneous rather than subcutaneous.
The gular division of the sensory canal system corresponds to the “gular line” of pit organs in Heptanchus,
Squalus and Mustelys,
The Anatomy of Chlamydoselachus 497
TABLE V.
CENOGENETIC CHARACTERS OF CHLAMYDOSELACHUS
Unusually elongate form of the body.
Weakness of the dermal fin rays.
Bunching of the pelvic, dorsal and anal fins near the caudal.
Unusually large mouth, and very distensible oropharyngeal cavity.
First pair of gill-covers enlarged, loose-fitting and frilled. They are continuous with a gular fold, unique
among sharks.
Abdominal or tropeic folds, unique among vertebrates.
Peculiar and imperfect hyostylism of the skull. The hyomandibular articular facet is very long, permitting
a gliding action.
Jaws are unusually long, and begin far posterior to the cranium.
Heterospondyly of the extreme caudal end of the vertebral column.
Shortness and irregularity (fragmentation, displacement, fusion) of cartilaginous fin rays (radials).
Infolding of the musculature of the ventral body wall in connection with the tropeic folds.
Alleged absence of an intermandibular muscle innervated by a branch of the trigeminal nerve.
Dorsal group of eye muscles much stronger than the ventral group.
Presence of an accessory musculus rectus lateralis.
All the recti muscles, save only a portion of the accessory rectus lateralis, take origin from the eyestalk.
Pyloric vestibule sometimes a sharply defined division of the digestive tube.
The middle intestine is expanded to form a bursa entiana.
Right and left lobes of the liver extend the entire length of the body cavity.
The gill-clefts are unusually large, and the respiratory surface afforded by the gills is great.
The external spiracular openings are very small.
Mesonephric duct, urinary sinus and urethral pore of the right side are often defective.
In adult females, the genital organs of the right side are much better developed than those of the left side;
the latter are probably not functional.
The young are retained in the uterus until they reach an advanced stage of development.
The anterior unpaired portion of the pericardio-peritoneal canal is very short and broad. The paired canals
often end blindly.
Afferent branchial arteries are connected by a series of loops over the gill-slits.
The connections between the acustico-lateralis elements of the fifth, seventh and eighth cranial nerves
show a tendency toward unification of the system.
Peculiar mechanism by which the eyes may be protected in the absence of lids,
498 Bashford Dean Memorial Volume
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Dean, BAsHForD
1894 Contributions to the morphology of Cladoselache (Cladodus). Journ. Morphol., 9, 85-115, pl.
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1909 Studies on fossil fishes (sharks, chimaeroids, and arthrodires). Mem. Amer. Mus. Nat. Hist., 9,
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Derneca, W. A.
1909 Contributions to the knowledge of the anatomy of Chlamydoselachus anguineus Garm. I. Skele-
ton [Russian text]. Trudy Sravnit. Anat. Instit. Imp. Univ. Moskva, no. 7, 66 pp., 4 pls.
1923 Zur Kenntniss der Anatomie des Chlamydoselachus anguineus Garm. I. Skelett. Bull. Soc.
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1903 The development of the head muscles in Scyllium canicula. Journ. Anat. Physiol., 37, 73-
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500 Bashford Dean Memorial Volume
Ewart, J. C., AnD Cotzg, F. J.
1895 On the dorsal branches of the cranial and spinal nerves of elasmobranchs. Proc. Roy. Soc.
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FERGUSON, JEREMIAH S.
1911 Anatomy of the thyroid gland of elasmobranchs, with remarks upon the hypobranchial circu-
lation in these fishes. Amer. Journ. Anat., 11, 151-210, 20 figs.
Froriep, AUGUST
1902 Zur Entwicklungsgeschichte des Wirbeltierkopfes. Anat. Anz. (Verh. Anat. Ges.), 21, 34-
46, 5 figs.
FURBRINGER, KARL
1903 _—-Beitrage zur Kenntnis des Visceralskelets der Selachier. Morph. Jahrb., 31, 360-445, 3 pls.
FURBRINGER, Max
1896 Ueber die mit dem Visceralskelet verbundenen spinalen Muskeln der Selachier. Jena. Zeitschr.
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1897 Ueber die spino-occipitalen Nerven der Selachier und Holocephalen und ihre vergleichende
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Gapow, Hans, anp Assortrt, E. C.
1895 On the evolution of the vertebral column of fishes. Phil. Trans. Roy. Soc. London, 186 B,
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GarMAN, SAMUEL
1884.1 An extraordinary shark [Chlamydoselachus anguineus]. Bull. Essex Instit., 16, 47-55, fig.
1884.2 A peculiar selachian [Chlamydoselachus anguineus]. Science, 3, 116-117, fig.
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1885.2 Chlamydoselachus anguineus Garman—a living species of cladodont shark. Bull. Mus. Comp.
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GEGENBAUR, CARL
1864-72 Untersuchungen zur vergleichenden Anatomie der Wirbelthiere. Leipzig.
1870 Ueber das Skelett der Gliedmassen der Wirbelthiere in Allgemeinen und der Hintergliedmassen
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The Anatomy of Chlamydoselachus 501
Goopry, T.
1910.1 A contribution to the skeletal anatomy of the frilled shark, Chlamydoselachus anguineus Gar.
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1910.2 Vestiges of the thyroid in Chlamydoselachus anguineus, Scyllium catulus, and Scyllium canicula.
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Goopricu, E. S.
1906 Notes on the development, structure and origin of the median and paired fins of fishes. Quart.
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1918.1 Development of pericardio-peritoneal canals in selachians. Journ. Anat., Cambridge, 53,
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1930 Studies on the structure and development of vertebrates. London, 837 pp., 754 figs.
Grecory, WittraM K.
1933 Fish skulls: a study of the evolution of natural mechanisms. Trans. Amer. Phil. Soc., 23,
75-481, 2 pls., 302 text-figs.
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1933 The natural history of the frilled shark, Chlamydoselachus anguineus. Bashford Dean Mem.
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GunrtHer, ALBERT
1887 Report on the deepsea fishes collected by H. M. S. Challenger during the years 1873-76.
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Harman, B.
1899 The palpebral and oculomotor apparatus in fishes: observations on morphology and develop-
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1906 The cranial and spinal nerves of Chlamydoselachus anguineus (Garm.). Proc. Zool. Soc. London,
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1907 On the abdominal viscera and a vestigial seventh branchial arch in Chlamydoselachus. Proc.
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Herrick, C. J.
1899 The cranial and first spinal nerves of Menidia: a contribution upon the nerve components of
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1900 Ueber die Entstehung der Scheidewand zwischen Pericardial und Peritonealhohle und tiber die
Bildung des Canalis pericardiaco-peritonealis bei Embryonen von Acanthias vulgaris. Morph.
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502 Bashford Dean Memorial Volume
Howe tt, A. Brazier
1933. Morphogenesis of shoulder architecture. Part. I. General considerations. Quart. Rev. Biol.,
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Howes, Grorce Bonp
1883. On the presence of a tympanum in the genus Raia. Journ. Anat. Physiol., 17, 188-190, pl.
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1872 Die Kopfarterien der Haifische. Denkschr. Akad. Wiss. Wien, 32, 263-275, 3 pls.
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1917 Structure and development of the sense organs of the lateral canal system of selachians (Mustelus
canis and Squalus acanthias). Journ. Comp. Neurol., 28, 1-74, 83 figs.
Joxnston, J. B.
1905.1 The morphology of the vertebrate head from the viewpoint of the primitive functional divi-
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Lanpacrg, E. L.
1916 The cerebral ganglia and early nerves of Squalus acanthias. Journ. Comp. Neurol., 27, 19-
67, 13 figs.
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1876 - Nuovi studi sopra ai pesci ed altri vertebrati fossili delle colline Toscane. Florence. (Chlamy-
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LeiGH SHARPE, WILLIAM HaroLp
1920 The comparative morphology of the secondary sexual characters of elasmobranch fishes—the
claspers, clasper siphons, and clasper glands. Mem.I. Journ. Morphol., 34, 245-266, 12 figs.
1926 The comparative morphology of the secondary sexual characters of elasmobranch fishes. The
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307-320, 15 figs.
LERIcHE, MAURICE
1929 Sur une forme nouvelle du genre Chlamydoselachus (C. tobleri) rejetée par le volcan de boue de
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55-58, 2 figs.
Luter, ALEXANDER FERDINAND
1909 Untersuchungen tber die vom Nervus trigeminus innervierte Muskulatur der Selachier (Haie
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1870 Beitrage zur vergleichenden Neurologie der Wirbelthiere. I. Das Gehirn der Selachier. II. Das
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1881 On the head cavities and associated nerves of elasmobranchs. Quart. Journ. Micr, Sci., 21,
72-98, 2 pls.
The Anatomy of Chlamydoselachus 503
Maurer, FRIEDRICH
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Mivart, St. GEORGE
1879 Notes on the fins of elasmobranchs, with considerations on the nature and homologies of verte-
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1785 The structure and physiology of fishes explained, and compared with those of man and other
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1911 Untersuchungen liber die Muskeln und Nerven der Brustflosse und der Kérperwand bei
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1897 The development of the hypoglossus musculature in Petromyzon and Squalus. Anat. Anz.,
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1918 The history of the eye muscles. Journ. Morphol., 30, 433-453, 20 figs.
Nisui, SEIHO
1922 Beitrage zur vergleichenden Anatomie der Augenmuskulatur. Arb. Anat. Instit. K. Japon.
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NisHikawa, T.
1898 Notes on some embryos of Chlamydoselachus anguineus Garm. Anmnot. Zool. Japon., 2, 95-102,
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1929 The distribution and innervation of the ampullae of Lorenzini of the dogfish, Squalus acanthias.
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1920 The cranial, occipital, and anterior spinal nerves of the dogfish, Squalus acanthias. Journ.
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~
Ossurn, RAyMonpD C.
1906 The origin of vertebrate limbs. Recent evidence upon this problem from studies on primitive
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1935 Organography of Gambusia patruelis (Baird and Girard). Journ. Morphol., 57, 303-316
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504 Bashford Dean Memorial Volume
Recan, C. Tate
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1875 Das Urogenitalsystem der Plagiostomen und seine Bedeutung fir das der tbrigen Wirbeltiere.
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1923 The caudal longitudinal collecting nerve trunks of elasmobranch fishes. Anat. Rec., 25, 23-
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1906 On the membranous labyrinth of certain sharks. Journ. Linn. Soc. London (Zool.), 29, 407-
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1876 Median and paired fins. A contribution to the history of vertebrate limbs. Trans. Conn.
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1883 Ueber die Mesodermsegmente und die Entwicklung der Nerven des Selachierkopfes. Verh.
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1874 Untersuchung zur vergleichenden Anatomie der Kiemen- und Kiefermuskulatur der Fische.
Jena. Zeitschr. Naturwiss., 8, 405-458, 2 pls.
Wiper, Burt G.
1905 On the brains of Scymnus, Mitsukurina and Chlamydoselachus, with remarks upon selachian
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The Anatomy of Chlamydoselachus 505
Woopwarp, ARTHUR SMITH
1921 Observations on some extinct elasmobranch fishes. Proc. Linn. Soc. London for 1920-1921,
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1905‘ The brain and cranial nerves of Bdellostoma dombeyi. Quart. Journ. Micr. Sci.,n. s. 49, 137-
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1908 Ein Embryo von Chlamydoselachus anguineus Gar. Anat. Anz., 33, 561-574, 7 figs.
ZiTTEL, K. von
1923 Grundztige der Paldontologie. II Abtheilung: Vertebrata. Munchen und Berlin. (Tooth of
Hybodus reticulatus, fig. 93).
PLANT e II
THE ANATOMY OF CHLAMYDOSELACHUS ANGUINEUS
ALN IO Il
THE CRANIUM OF CHLAMYDOSELACHUS, WITH THE ANTERIOR END OF THE
VERTEBRAL COLUMN ATTACHED
Fig. 1. Dorsal view of the cranium, natural size.
af, articular facet for hyomandibular; an, ala nasalis; cb, cavum precerebrale; ecb, ectethmoidal process; ef, endolym-
phatic fossa; es, eyestalk; fp, foramen for nervus profundus; id, interdorsal; pc, preorbital canal or foramen; pop,
postorbital process.
After Allis, 1923, Fig. 9, pl. VIII.
Fig. 2. Ventral view of the cranium, natural size.
dop, antorbital process; ba, bulla acustica; fic, foramen for internal carotid artery; fso, foramina supraorbitalia; naf, nasal
fontanelle; pb, palatobasal ridge.
After Allis, 1923, Fig. 11, pl. IX.
Fig. 3. Lateral view of the cranium, natural size.
af, articular facet for hyomandibular; bd, basidorsals; fe, foramen for efferent pseudobranchial artery; ff, foramen for
nervus facialis; fic, foramen for internal carotid artery; fo, foramen for nervus opticus; foc, foramina for occipital nerves;
fom, foramen for nervus oculomotorius; fp, foramen for nervus profundus; ftr, foramen for nervus trochlearis; id, inter-
dorsals; n, nodule of cartilage; naf, nasal fontanelle; onc, orbitonasal canal; pb, palatobasal ridge; pc, preorbital canal, or
foramen; 7, rostrum; sbd, supra-basidorsals; tpf; trigemino-pituitary fossa.
After Allis, 1923, Fig. 8, pl. VIII.
Dean MemortaLt VoLuME Articte VI, Prate I
PAVE aul
THE ANATOMY OF CHLAMYDOSELACHUS ANGUINEUS
LAL NIN, II
THE CRANIUM AND PORTIONS OF THE VISCERAL SKELETON
OF CHLAMYDOSELACHUS
Fig. 4. | Medial view of cranium and anterior end of the vertebral column, natural size.
an, ala nasalis; bd, basidorsals; ef, endolymphatic fossa; fe, foramen for efferent pseudobranchial artery; fgl, foramen for
nervus glossopharyngeus; fic, foramen for internal carotid artery; fo, foramen for nervus opticus; foc, foramina for
occipital nerves; fol, foramen for nervus olfactorius; fom, foramen for nervus oculomotorius; ftr, foramen for nervus
trochlearis; fv, foramen for nervus vagus; id, interdorsal; nc, notochord; pb, palatobasal ridge; pv, canal, or foramen, for
pituitary vein; 7, rostrum; tf, acustico-trigemino-facialis recess.
After Allis, 1923, Fig. 12, pl. IX.
Fig. 5. Lateral view of cranium, with jaw cartilages and hyoid cartilages attached, natural size.
i=)
al, anterior upper labial cartilage; an, ala nasalis; aop, antorbital process; ch, ceratohyoid; ecp, ectethmoidal process;
es, eyestalk; g( = gamma), the process corresponding to Addy of Vetter’s (1874) description in other selachians; hmd,
hyomandibular; Imh, ligamentum mandibulo-hyoideum; md, mandibular; ml mandibular labial cartilage; n, nodule of
cartilage; naf, nasal fontanelle; orp, orbital process of palatoquadrate; pl, posterior upper labial cartilage; pop, postor-
bital process; pq, palatoquadrate.
After Allis, 1923, Fig. 7, pl. VII.
Fig. 6. Posterior view of the cranium, natural size.
af, articular facet for hyomandibular; ecp, ectethmoidal process; es, eyestalk; fm, foramen magnum; guf, glossopharyngo-
vagus fossa; pop, postorbital process.
After Allis, 1923, Fig. 10, pl. VIII.
Dean Memorial VOLUME Articte VI, Prate II
i
i
|
t
'
LAs JUUL
THE ANATOMY OF CHLAMYDOSELACHUS ANGUINEUS
ALANIS JOU
THE BRAIN AND PORTIONS OF THE VISCERAL SKELETON OF CHLAMYDOSELACHUS
Fig. 7. Dorsal view of the brain and cranial cavity, natural size.
a, artery; 0, nervus opticus; ocm, n. oculomotorius; ol, tractus olfactorius; tr, n. trochlearis; v, vein.
After Allis, 1923, Fig. 59, pl. XXII.
Fig. 8. Dorsal view of the branchial arches, natural size. The branchial rays related to the ceratobranchials
have been removed.
bbr2, second basibranchial; bbr5—6, fused fifth and sixth basibranchials; bh, basihyoid; cb1, musculus coracobranchialis
of the first arch; cbr1, ceratobranchial of the first arch; cbr6, ceratobranchial of the sixth arch; ch, ceratohyoid; ebr1,
epibranchial of the first arch; ebr6, epibranchial of the sixth arch; hbr2, hypobranchial of the second arch; pbr5, pharyngo-
branchial of the fifth arch.
After Allis, 1923, Fig. 35, pl. XIII.
Fig. 9. | Ventral view of the median portion of the branchial skeleton, natural size.
bbr3, basibranchial of the third arch; cbr6, ceratobranchial of the sixth arch; ch, ceratohyoid; hbr2, hypobranchial
the second arch.
After Allis, 1923, Fig. 36, pl. XIII.
Dean Memoria VOLUME Articte VI, Pirate III
LANE, IY
THE ANATOMY OF CHLAMYDOSELACHUS ANGUINEUS
PEATE ANY
EYE MUSCLES, BRAIN, VALVULAR INTESTINE AND DUCTUS DEFERENS
OF CHLAMYDOSELACHUS
Figs. 10, 1l and 12. The eye muscles and their nerves, excepting the nervus abducens which innervates
the external rectus muscle.
The explanation of the labels is combined with that for the next two figures.
After Hawkes, 1906. Figs. 4-6, pl. LXIX.
Figs.13 and 14. Dorsal and ventral views of lateral halves of the brain, showing roots of cranial nerves.
II, optic nerve; III, oculomotor nerve; IV, trochlear nerve; V, VII, the united Gasserian and buccalis ganglia; VI,
nervus abducens; VII b., ramus buccalis; VIIh., truncus hyomandibularis; VIII, the ganglion of the eighth nerve; LX,
glossopharyngeal nerve; X, vagus nerve.
A.B., anastomosing branch between the oculomotor and profundus nerves; C., ciliary branch of the profundus; Cer.,
cerebellum; Hy., hypophysis; I.O., inferior oblique muscle; L.I., lobi inferiores; Lin.Lat., lineae laterales or restiform
bodies; L.N., Locy’s nerve (nervus terminalis); Oc.1,2,3, first three spino-occipital nerves; Op.S., optic stalk (cartilago-
sustentaculum oculi); Op.L., optic lobes; O.S., olfactory stalk; Pro., profundus branch of fifth or trigeminal nerve;
Pros., prosencephalon; R.Ext., A and B, two parts of the rectus externus muscle; R-In., rectus internus muscle; R.Inf.,
rectus inferior muscle; R.S., rectus superior muscle; S.Ob., superior oblique muscle; S.V., saccus vasculosus.
After Hawkes, 1906, Figs. 7 and 8, pl. LXIX.
Fig. 15. Valvular intestine slit open to show the spiral valve and the thick muscular wall.
After Ginther, 1887, Fig. 5, pl. LXV.
Fig. 16. Lower part of left ductus deferens (vas deferens) opened longitudinally to show “annular” folds.
After Ginther, 1887, Fig. 4, pl. LXV.
Articte VI, Prate IV
Dean MemoriaL VOLUME
PEAMERY
THE ANATOMY OF CHLAMYDOSELACHUS ANGUINEUS
Fig.
Fig.
Fig.
17.
18.
= 19)
ig. 21.
22.
PEER)
THE UROGENITAL ORGANS OF CHLAMYDOSELACHUS
External (ventral) view of the cloaca and abdominal apertures in a normally developed male.
cl, cloaca; po, porus abdominalis; ug, urogenital openings; v, vent.
After Ginther, 1887, Fig. 1, pl. LXV.
External (ventral) view of the cloaca and abdominal apertures in an asymmetrically developed
male. The ducts of the right side are not so well developed as those of the left.
cl. cloaca; po, porus abdominalis; ug, urogenital openings; v, vent.
After Ginther, 1887, Fig. 2, pl. LXV.
Side view of the ductus deferentia (vasa deferentia) of a specimen with unequal development of
the genital ducts. Compare preceding figure, drawn from the same specimen.
gl, gland; i, rectum opened; po, porus abdominalis; r, kidney; u, urinary bladder; ug, right, and ugl, left urogenital
opening; vd, left, and vd1, right ductus deferens.
After Ginther, 1887, Fig. 3, pl. LXV.
Ventral view of pelvic fins, myxopterygia and cloacal aperture of a 1474-mm. male.
After Ginther, 1887, Fig. C, pl. LXIV.
Dorsal view of the right half of the pelvic girdle and endoskeleton of the right pelvic fin of a male.
B., basipterygium; b., axial cartilage; bl, intercalary cartilage; Be. [beta], modified radial; I.n-f., longitudinal nerve
foramen; p.g., pelvic girdle; 7 lateral radials; Rv. marginal ventral cartilage; T.d., terminal dorsal cartilage; T.v.,
terminal ventral cartilage.
After Goodey, 1910.1, Fig. 22, pl. XLVI.
ote view of the pelvic fin and the right half of the pelvic girdle of a male, showing musculature.
A., adductor muscle; B., basipterygium; Be.[beta], modified radial; c.n., collector nerve; D., dilator muscle; Fl.e.,
musculus flexor externus; Fl.i., musculus — internus; I.r., last lateral radial; O., dorsal radial muscles; p.g., pel-
vic Bice, Rv., marginal ventral cartilage; S., compressor muscle; Teds terminal dorsal cartilage; T.v., terminal
ven cartilage.
After Goodey, 1910.1, Fig. 20, plate XLVI.
Ventral view of the pelvic fin represented in Figs. 21 and 22, showing muscles.
Fl.e., musculus flexor externus; Ra., ventral radial muscles; S., compressor muscle; T.v., terminal ventral cartilage.
After Goodey, 1910.1, Fig. 21, pl. XLVI.
Articte VI, Prate V
Dean MeEmorIAL VOLUME
p=
ag OS, 7
Si
/
&
Les, WAI
THE ANATOMY OF CHLAMYDOSELACHUS ANGIUNEUS
Fig. 24.
Fig. 25.
Fig. 26.
Fig. 27.
RIP AW EDA
THE BRAIN OF CHLAMDOSELACHUS
The brain in dorsal view and in transverse sections taken at various levels.
Ventral view of the brain of the frilled shark.
The brain of Chlamydoselachus in lateral view.
Vertical longitudinal section of the brain of Chlamydoselachus.
1, olfactory lobe; 2, nervus opticus; 3, oculomotorius; 4, trochlearis; 5, trigeminus; 6, abducens; 7, facialis; 8, acusticus;
9, glossopharyngeus; 10, vagus.
These figures are reproduced from the original drawings by Paulus Roetter for Garman, 1885.2, Pls. XV and XVI.
Dean MemortaL VOLUME Articte VI, Prate VI
leben, \AUL
THE ANATOMY OF CHLAMYDOSELACHUS ANGUINEUS
ALAIN YU
NERVOUS SYSTEM AND CERTAIN SENSE ORGANS OF HEPTANCHUS
AND CHLAMYDOSELACHUS
Fig. 28. Brain, cranial nerves and associated sense organs of Heptanchus maculatus, dorsal view.
bu. VII, buccal branch of facial nerve; cb., cerebellum; cl., ciliary nerve; c.r., restiform body; hmd., hyomandibular
division of the facial nerve; md. V, mandibular division of the fifth nerve; m.n., median olfactory nucleus; med., medulla;
mx.V, maxillary division of trigeminal nerve; ol.b., olfactory bulb; ol.l., olfactory lobe; ol.t., olfactory tract; op.l.,
optic lobe; op.V, ophthaimicus profundus division of the trigeminal nerve; os.V and VII, ophthalmicus superficialis
of trigeminal and facial nerves; tl., telencephalon; tn., terminal nerve; y-z, occipitospinal nerves: I, olfactory nerve; II,
optic; II, oculomotor; IV, trochlearis; VI, abducens; VIII, auditory; IX, glossopharyngeal; X, vagus.
After Daniel, 1934, Fig. 200a.
Fig. 29. Diagrammatic drawing of the cranial nerves and lateral line canals of Chlamydoselachus.
B.A., buccal ampullae; Bucc., ramus buccalis VII; C.F., general cutaneous fibres going to skin; Con.V5, nerve strand
connecting the pre- and post-trematic rami of vagus 5; Con. V6, nerve strand connecting vagus 6 with a spinal nerve;
D.G., dorsal branch of the glossopharyngeus, dividing into a cephalad branch which passes to the neuromasts, and
a caudal branch whose distribution is undetermined; E.M. (VII)(A,B,C,D,E), the five parts of the externus mandibularis
VII; H., the ganglion of the truncus hyomandibularis, i.e., the true ganglion of the facialis, combined with one of the
acustico-lateralis ganglia; H.A., hyoid ampullae; H.L.(A,B,C), the hyomandibular lateral line canal and its three main
branches; H.M., the common trunk of the ramus hyoideus and ramus internus mandibularis VII; I.(A,B,C), the three
principal rami intestinales; I.H., the cardiac branch of the ramus intestinalis; I.M.VII, ramus internus mandibularis
VII; L.O.L., infraorbital lateral line canal; L.L., main lateral line canal; Mxb., branch of the maxillaris which becomes
united with a branch of the buccalis; Mxb.b., two fine nerves which appear to originate from a branch of the buccalis,
but which are composed of general cutaneous fibers which have come from Mxb.; P., palatine branches of the facialis;
P.B.A., posterobuccal ampullae; Pr.F.(ch.), the chorda tympani; Pr. and Pt., the pre- and post-trematic rami of IX and
of the vagus; Pro., profundus branch of V; Pt.F., post-trematic facialis; R.H., ramus hyoideus VII; R.Man.V, ramus
mandibularis V; R.Max., ramus maxillaris V; R.O., ramus oticus with cutaneous branches R.O.C.; S.(1,2,3,4,5,6,7,8),
the first eight spinal nerves; s.h.(1,2), the two branches which make up the hypoglossal nerve; S.O., occipitospinal
riband; S.O.A., supraorbital ampullae; S.O.L., supraorbital lateral line canal; S.Op.V, superficialis ophthalmicus V;
S.Op. VU, superficialis ophthalmicus VII; T.H., truncus hyomandibularis; V(1,2,3,4,5,6), the six branchial branches
of the vagus; V.G., visceralis branch of IX; Vis., visceralis branches of the vagus; V, VII, the united Gasserian and
buccalis ganglia; IX, IXg., the glossopharyngeal nerve and its ganglion; X, Xg., the vagus nerve and its composite
ganglion, ae and X.B, dorsal branches of the vagus to neuromasts. The remaining abbreviations are not explained
by the author.
After Hawkes, 1906, Fig. 1, pl. LX VIII (in color).
Fig. 30. Right membranous labyrinth (x 2) of Chlamydoselachus, medial aspect.
The explanation of the labels is combined with that for the next figure.
After Goodey, 1910.1, Fig. 7, pl. XLIII.
Fig. 31. Right membranous labyrinth (x 2) of Chlamydoselachus, lateral aspect.
a.a., ampulla anterior; a.d.e., apertura ductus endolymphaticus externus; a.e., ampulla externus; a.p., ampulla posterior;
c.a., canalis anterior; c.e., canalis externus; c.p., canalis posterior; d.e., ductus endolymphaticus; d.u.s.p., ductus
utriculo-saccularis posterior; |., lagena; p.f., parietal fossa; r.a.a., ramus of eighth nerve to ampulla of anterior canal;
7.a.e., famus to ampulla externus; r.a.p., ramus to ampulla posterior; rec., recessus utriculi; 7.1., ramus to lagena; r.n.,
ramus to macula neglecta; 7.s., ramus to sacculus; 7.u., ramus to utriculus; s., sacculus; s.e., saccus endolymphaticus;
t., tympanic aperture; u.a., utriculus anterior; u. p., utriculus posterior; VIII, eighth cranial nerve.
After Goodey, 1910.1, Fig. 8, pl. XLIII,
Dean MemortiAL VoLuME Articte VI, Prate VII
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Pont ORD DEAN MEMORIAL VOLUME
ENNCoIAC Jelisleles
Edited By
EUGENE WILLIS GUDGER
Articie VII
THE BREEDING HABITS, REPRODUCTIVE ORGANS
AND EXTERNAL EMBRYONIC DEVELOPMENT
OF CHEAMiDOSERACEHOS, BASED ON NOTES
AND DRAWINGS BY BASHFORD DEAN
By E. W. GUDGER
Honorary Associate in Ichthyology
American Museum of Natural History
NEW YORK >
PUBLISHED BY ORDER OF THE TRUSTEES
Issued October 15, 1940
ARTICLE VII
THE BREEDING HABITS, REPRODUCTIVE ORGANS, AND
EXTERNAL EMBRYONIC DEVELOPMENT OF CHLAMYDOSELACHUS,
BASED ON NOTES AND DRAWINGS LEFT
BY BASHFORD DEAN
By E. W. Gudger
CONTENTS
ING R'OD UW CTIO NA ee eee te eae arco cree! cs sacl etoe an its ee 525
SIRES SPECIMENS PANDA DHEIRT SOURCE NNN Aa nce ian Ale een ener oS 27)
Date IDRARAIES AIio) Ii ANUABSONGSNID, . 5 ono once ened ono uooseunssuaddonuce 529
Viviparity (Ovoviviparity) IN Chlamydoselachus................-.0...00-. 531
BREEDING SEASON OE LEHE LP RIEEEDLO HAR Kanes Slr nr ee aia on) a ee 534
EWAIDENGESER OMETEE| OVARIES pan eae toate ee ere eee ye era acer 534
STAGESKO ESE NIB RSYOSBINEISETEN O55 Rae ea emer Pn en 535
DuRATION OF GESTATION aS OST EOS Ee OO OMA SCROLL AIT GSES EO OL Oa Ga oh fOCOREn Crt ce Sat Eeorc sree eee sie 538
Tue REPRODUCTIVE ORGANS OF THE Mate Chlamydoselachus.................. 541
MyxorTeRYGIA—EXTERNAL ORGANS OF THE MALE..................- 000000 e eee sees 541
Tue REPRODUCTIVE ORGANS OF THE FEMALE Chlamydoselachus................ 542
BIRFTES @) W/AVRITES ROPe eh oy ee ety Tete A HOUR ir ic er PRO ER DPOReae th Oem tH cn le re AG UR ae aa 544
TMMCATUR ETO VARTANAEGGSAN AA eae alee var erieg era Ee eeatate RGR Meson ALI BRE LS ecole 548
VARNAATRURE | OWARTANGE GG Ay eco freee eo CR eT SE NST SEY IDR oe Poe ou Cae se 548
BIRETRS QV TDW CSE toes eee ae ee eae arr aly ECS Pea MSC Re Tee Ure clin aR ar Ste 549
THE WABDOMIN AD © PENINGS i batccra lacie Sct err OIE CHES eps e are ee tinicen ees gee noe Tey Perea 549
SIME SHELTS GUA NDS oe heen c= cnisieceraiecper tage een SRT al ME SAP Salt gah et aah deers oe Bi ee Sa Ney Me 550
FISHES TER USS sete ester eee ee Gee nor oon Te tar Te ch ee Ne ate Ge pene encr ois et eet see 552
RicHTAWTERUSHRUNCTIONAL MEE eee enicee rine Pee SAR a ae Sate ah ue TARE 552
Lerr Urerus SOMETIMES FUNCTIONAL...............-0--+05- ERT ae ALTE eae Te 557
Do Emsryos Receive NuTRIMENT FROM Uterine WALL?.............--- 0-2-2 eee eee 559
Tue Croacar Openincs. PAO ae tek Vegettidt oo cot a eee ROG ge ROR UR 5 IMRT NPN bE 562
Ree a Gene cae meee: Sey eee Artes ees 562
FEMALE REPRODUCTIVE ORGANS OF ene nee anaes AND Wanton: Rae . 564
@VARIES AND) ©viDUCTS OF SOME) FLORIDAU SHARKS) »....05--425 000 0se so snes sss ee eee: 564
OWARIES AND O\nmiiens Ox WANROURIRNB. coo cncnucoeuoucccuccn ceo oanunbnveec ee 565
arESENCAPSUDEDIEGGIOER Chlamydosclachusm =e) ae eee ee 566
ERE TOMDVAL, ESS Oi INsny JOT NAD) EVN, 525664 0ncudonogocuscacodndvendcueuvene sed 567
Normat Etiipsoipat Encapsutep Eccs..............-.-.-..-- FE COT ae Tae ee eee 567
Unusuat Exzipsorpar Eccs with TENDRILIFORM Processes.......... SF ay my ee Preten te seat 569
JANSECLIPDICATIE GG REESE EE eee: NS ised cd Ae EN ned eae eer ChE ee 569
Some Ostone Ferrite Eccs...........-...-- ne: ag ar a ARE MEU ey 6 570
An Etoncate Inrertive (Wind) Ecc..............-..-- EEE Ae ee etre ME OPIS Bee ae 571
IROUNDIECCSIOE CHE MRIDUEDIOHAR Kei saree ene rie Sci cie iets reece 572
Sizes or Eccs or Chlamydoselachus CoMPARED WITH THOsE OF OTHER SHARKS..........-- 573
Sizes or Eccs AND EMBRYOS OF THE FRILLED SHARK.......... Pe et en on Oy ee 573
SizeslOPEGGS/ANDIE MBRYOs|OF)ISURIDI SHARKS eee incieeinieit tei ines isiee 574
SIzEstORIEGGS|OELTHERNIURSE: SETA R Kept St este ne eam et a Ora wa 576
ForMATION OF THE Eco Capsutes oF Chlamydoselachus AND OF Ginelymoscomna | ee ree 578
FORMATION OF TENDRILIFORM PROCESSES... .....0 0: -¢ eee nec deeeee ces Beg a nied Hae sede 579
ExTERNAL EmpBryonic DEVELOPMENT OF Chlamydoselachus....................
Earty DEVELOPMENT
Résumé or RESEARCHES ON THE INTERNAL DEVELOPMENT.........-.-2-+-2-02--0 eee e eee eeeeee
IDESCRIETIONS OF EMBRYOSIRIGURED eae ene rate es ee eee
Tue Avutt Chlamydoselachus
An Aputt FEMALE FRILLED SHARK
Aw Aputt Mate Chlamydoselachus
Heap On ty of THE ADULT SHARK
ExTERNAL GILL-FILAMENTS OF Chlamydoselachus
ExTERNAL GILL-FILAMENTS OF THE EMBRYO
(ANIEMBRYO\OFS IES ONIDEIMETERS 4 ce, says ae ois acts =) = eaten eo eee
An Emsryo 15.5 wot. iN LENGTH................
IANJEMBRYOPMIEASURING)2O) NAILETMETERS pee eter tora ete coer
Two 25-m™. Empryos—Heaps Onty—Descrisep sy ZIEGLER AND BROHMER
INISHIKAW.ANS}3 22MM EMBRYO—— HEAD) ONLYase eee oan eee eee
DEAN SIEMBRYO:/ 34 MMINIEENGTH Ac cian ck ieieic sae aie © OC OR OEE Erne eon
Aw Empryo oF 39 MILLIMETERS... ....
SRE OMA MBRYOZANDILTS YOLKS OAC INI COLOR=E PE eee et en een nny eee
NisHIKAWA’s 43-mMM. EmMBryO ON ITs YOLK SAC ...............
DEAN'S EMBRYO (OF146 QAILLIMETERS & <=, c= Spo 5 2 cv SS apes oe ees ee ee eee I ee
IFIED ORFAC4 52 NEM) SPEC IMENGSIN (A VENSER A Tn VTE Wy oar
INISHIK-AW/AGS 5 OzMMep EE MBRY OLONILTS PY OLESOA Cee ee
/ANVEMBRYO) OF S45 MILLIMETERS op ooyge enc Py sen tetas en ee ds de era CT a
/ANJEMBRYOMMEASURING O59) MILLIMETERS Se ay ee 2 ee eee ar ince eee ee
GARMANS! EMBRYOIOF{64) MIDLIMETERS psy Gey ee eee oe
DEAN|S EMBRYO) MEASURING 66) MIELIMETERS Sei eee eee eee eee ee
(ANS EMBRYO}103 UMMEINS EENGTHi is oes er eee en Oe eee
JANI EMBRYOIOBRHL24 MOCETMETERS feo oh5/ f= cus /5).s0c) ccky 3cooees ci Sehr Oe ee tenons
ZANTE MABRY O{OEs1// DIMM VANDILES HY OLRIO AC Hen ey errno eT nee Sie va
AN TEMBRYO1 85) MM) INVCENGDH Se Wa e an eae eae pe oP eee Reena eee ence ree eee ee ee
ACY OUNG ERTELED SHARK! 240) MOM LONG otc Pi worl aa eee oS Sapa
ZAV390-aasts) Chlamydoselachusiines NATURAL COLORSERE EE Soe eee reesei eee
THE YOLK SAG CIRCULATION: Ae ee See oe ee ee ae eee ae ee
WITELEINE | @iR CULATION OF-EHE SG O2MMa EMBRYO meee aaerr te eee eae ean eee
SYOLK- SAC) CIRCULATION) OF-THE(43200Ma, OFECIMEN See ee et
MiITEELINE/ CIRCULATION] OFTHE 07MMa EMBRYO Pee ee nee
WOEK—SAC] CIRCULATIONIOR THEM / 54 Meie) RISE pee ee ee
WiIITELLINE: CIRCULATION OBETHE O00 zsN04, LAR Kae ee ee
THE BREEDING HABITS, REPRODUCTIVE ORGANS, AND
EXTERNAL EMBRYONIC DEVELOPMENT OF CHLAMYDOSELACHUS,
BASED ON NOTES AND DRAWINGS LEFT
BY BASHFORD DEAN
By E. W. Gupcer
Honorary Associate in Ichthyology
The American Museum of Natural History
INTRODUCTION
While on a leave of absence from Columbia University, Prof. Bashford Dean spent
parts of 1900 and 1901 in Japan. There he collected and studied many rare and little
known marine animals—particularly certain archaic fishes and their eggs and embryos.
That these collections were extensive, we know since there is a letter by him stating that
when shipped to America by freight they filled seven cases. In this shipment were
several adult frilled sharks, and others were sent to him later. Of the disposition of these
and of Dean’s generosity in sending specimens of this fish to various European investi-
gators, Gudger and Smith have written (1933, pp. 250-252).
Dean’s embryological materials were collected to enable him to follow and to il
lustrate the early life histories of two primitive elasmobranchs—the frilled shark, Chlamy-
doselachus anguineus, and the Port Jackson shark, Heterodontus (Cestracion) philippi.
Back in America, Dean found gaps in his materials and figures, so he returned to Japan and
did further work on these fishes during the months from May to October, 1906. Further-
more, other frilled-shark material was still later collected in Japan and sent to him in
America. I have records of specimens received by Dean on February 10, 1911, and on
January 13,1912. Ihave been unable to trace these specimens, but other lots came to him
and were deposited in the Dean collection in the zoological museum of Columbia Univer-
sity. Among the specimens loaned from Columbia are four lots of young embryos without
yolk sacs labelled “Bought in Tokyo Market, February 4, 1913; April 4, 1913; January 22,
1914; April 23, 1917”. His Japanese collectors evidently found the fresh-caught adult
sharks in the Tokyo market, opened the fish, cut the embryos from the uterine eggs,
and sent these embryos to Dean.
Since the above was written, I have learned that in 1917 Dr. Dean paid a flying visit
to Japan to collect armor and objects of art for the Metropolitan Museum of Art, in
which he was at that time curator of arms and armor. He reached Japan on March 28 and
embarked for the U.S. on May 19. This I have from a member of the party and from
his letters to Mrs. Dean. Hence he was in Japan when five embryos (to be referred to
later) were collected on April 23. These and the ones referred to above, were obtained
by his friends (whom he names in these letters), and preserved for him. The specimens
collected in 1917 (and possibly the others listed with them) were brought back by him in
May-June of that year.
526 Bashford Dean Memorial Voume
Among the embryological records accumulated by Dr. Dean during these two trips
and left unpublished at his death, are numerous drawings showing various stages in the
development of the primitive shark, Chlamydoselachus. In keeping with the plan and
purpose of this volume, as briefly set forth by Gudger and Smith on page 49 of Article I,
the present contribution has been prepared in order to preserve for science these excel-
lent drawings.
This article (No. VII) forms the third and last of a series dealing with this rare
shark. In the first, Gudger and Smith (1933) brought together from widespread sources
everything then known concerning the natural history of the fish, to form a background
for work on the anatomy and the embryology. Next came Dr. B. G. Smith’s monograph on
the anatomy. This includes a review of the results of many investigators, but to these
studies, Dr. Smith added the results of his own investigations on certain organ systems
either wholly or partly omitted by other writers. Smith’s dissections, it is interesting to
note, were done on specimens obtained in Japan by Dean.
And now there are set before me two tasks. The first is to make a study of Dean’s
notes on the breeding habits and seasons and on the structure and functioning of the re-
productive organs of the frilled shark. These notes are few, fragmentary and scat-
tered throughout a notebook marked CHLAMYDOSELACHUs and in various loose notes,
sketches and photographs. However, I have been able to piece together from Dean’s
notes, from the specimens loaned from Columbia University, and from the scanty litera-
ture, sufficient data to extend considerably our knowledge of these subjects. I am fortu-
nately able to bring forward for comparison data from my observations on the breeding
habits and genital organs of various sharks and rays, and particularly of the nurse shark,
Ginglymostoma cirratum, whose reproductive habits and large shelled eggs are remarkably
like those of Chlamydoselachus.
My second task is to prepare descriptions and explanations of the admirably drawn
figures of the eggs and embryos of this shark left unpublished by Dr. Dean at his untimely
death. For reasons to be given later, it will be clear why these figures do not portray
a completely graded series of embryos but only such stages as were procurable with great
difficulty. But before beginning the consideration of these drawings, other and intro-
ductory studies of the fish must be made.
Almost nothing has been published about the breeding seasons and breeding habits
of the frilled shark and equally little concerning the functioning of the reproductive organs.
Even less is known about the development of Chlamydoselachus. But when the breeding
habits and seasons and the reproductive organs have been studied and the figures of the
embryos described, the reader will have a fair idea of the life history of the frilled shark.
Some years before his death in 1928, Dr. Dean asked me to collaborate with him in
preparing an article such as this. But having much work planned for years ahead, | pre-
sented my case, and, Dean, generous as always, withdrew his request and urged me to
proceed with my own studies. And now that he is gone, I am trying to do what could
have been done long ago so much better in collaboration with him, since his memory
The Embryology of Chlamydoselachus Si]
would have supplied details not recorded among the very few notes available.
In this difficult task, I have been fortunate in having the active help and cooperation
of Dr. B.G. Smith. It isa pleasure to acknowledge my large obligation to him.
THE SPECIMENS AND THEIR SOURCE
That the collecting of eggs and embryos of Chlamydoselachus was not the main
object of Dean’s first visit to Japan, and that the finding of these eggs was somewhat un-
expected, it attested by this statement (Dean, 1901.1)—“‘My first object in visiting Japan
[in 1900] was to secure the eggs and embryos of the Port Jackson shark [Heterodontus =
Cestracion|.” The eggs of Heterodontus were found among rocks and seaweed in shallow
water, and were easily collected by divers and maintained without difficulty in aquaria of
running water or in floats in the sea. Hence it is not surprising that Dean procured
a fairly complete series of early stages of the embryos of this shark and that he devoted
most of his time to their study. The drawings of the eggs and embryos of Heterodontus,
which are more numerous than those of Chlamydoselachus, will form the basis of the final
article in this Memorial Volume.
139 5 lo 15° 20 25) 30 35° 40) 45
7 aes Lr T T T =F ot T Ua T T
26} GULFo TOKYO
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SAGAMI BAY 4
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g CENTRAL BASIN &
Re
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= thy.
SAGAM/I SEA Sig ra
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139° s 10 15° 20° 25° 30° 35° 40° 4s"
Text-figure 1
A map of the Sagami Sea, the Miura Peninsula, and part of the Gulf of Tokyo, showing the position of
the Misaki Laboratory in which Doctor Dean worked, and the waters from which his specimens of
Chlamydoselachus were obtained.
From an old chart compiled by Prof. I. Ijama.
528 Bashford Dean Memorial Volume
Dean knew of Garman’s monograph on the anatomy of Chlamydoselachus (1885) and
of Nishikawa’s pioneer work (1898) on the breeding habits and embryology. But in 1901
he wrote: “I hardly had hopes ... of obtaining [at Misaki] a series of embryos
fof Chlamydoselachus] . . . on account of its great rarity; for one could easily count on
his fingers all of even the adult specimens which had hitherto been brought from
Japan. . . I found, however, that . . . if one could secure many adult specimens there was
a fair chance of obtaining embryos, since this shark was known to be viviparous.”
During his twelve months in Japan (1900-1901), an intensive search for Chlamy-
doselachus was carried on. During his temporary absence from Misaki, this search was
prosecuted by his assistants, and, even after his departure for the United States, the hunt
was kept up—certainly as late as 1917. But so rare was the fish that in 1904, Dean wrote
that “*. .. in the course of a year, the neighborhood [the Sagami Sea] yields about a dozen
specimens [of both sexes]. And in his notebook under the heading “Abundance” is
this statement “1904. About 6—1 gravid”. In another place is this notation— 1905.
Kuma fished for about 5 weeks in the best ground off Odowara—special tackle—squid
bait, depth from 300-600 fathoms, took 3 fish” —one male and two females. The scarcity
of specimens and the difficulty of procuring them, it may be noted, is due to the fact that
they have to be fished for with trawl hooks at depths averaging from 1200 to 3600 feet.
Although 10 adult specimens of Chlamydoselachus have been taken in the seas of
western Europe, the only region where embryos have been obtained is still the Sagami
Sea, more particularly the waters around the Miura Peninsula on which the Misaki
Biological Station is situated. Dean states that he had females with young from Sagami
Bay (and particularly from the Odowara Maye); while other materials came from the
Gulf of Tokyo—another arm of the Sagami Sea. For these localities see Text-figure 1.
The chief collector at the Misaki Station in Dean’s day and for long afterwards was
Kuma Aoki, an ex-fisherman, who had a remarkable knowledge of all the specific localities
where Chlamydoselachus might be found. In addition to fishing directly for Dean, Kuma
made arrangements with other fishermen in. Sagami Bay that all frilled sharks taken by
them should be brought to the laboratory. Also Prof. Mitsukuri of the Imperial Uni-
versity of Tokyo arranged with the market people in Tokyo that all specimens brought
there from any source whatever should at once be sent to the station at Misaki. From all
these sources, material slowly came to Dean at the laboratory on the Miura Peninsula.
In the fragmentary entries in various handwritings in Dean’s notebook, a total of 42
adults are listed —16 males and 26 females. These cover the years 1900-1906 inclusive.
In Dean’s own handwriting, there are listed with measurements 21 adult fishes—7 males
and 14 females. I surmise that these were the results of Dean’s collecting for the 12 months
of 1900-1901. It is probable that the grand total of 42 adults, from all records in various
handwritings in his notebook, contains a number of duplications. Of the 26 females
listed, 10 are credited with producing 56 eggs. For 24 of these eggs it is stated that two
were in the blastula stage, two in the gastrula, while 20 had on them embryos varying
from 11.5 to 390 mm. in length.
The Embryology of Chlamydoselachus 529
The difficulty of arriving at a total for these eggs and embryos is due to the fact that
these notes were made by at least two other persons besides Dean. The table in Dean’s
handwriting recording 21 adults must have been compiled from various other entries
in the notebook labelled CHtramrposeLacuus. Finally, the matter is complicated by
the fact that the entries cover the catches of the years 1901-1906 inclusive. Here it
must be noted that between Dean’s departure from Japan in 1901 and his return in 1905,
specimens of adults and embryos were collected and sent to him in America. Some of
these are listed separately in the notebook referred to.
There was another small but valuable lot of material made available to Dean. A
young Japanese student, T. Nishikawa by name, had in May, 1896, collected eggs and
embryos of Chlamydoselachus. By June, 1897, he had finished a brief but interesting
paper (“Notes on some embryos of Chlamydoselachus anguineus Garman”). This was
published in 1898. In 1900, Dean at Misaki began to get eggs and embryos of the same
shark. Nishikawa, having finished with his materials and having published his article,
turned over to Dean all his specimens and slides to further Dean’s researches. Evidence
of this will be adduced in various sections of this article to follow.
Of the embryological material brought back by Dean in 1901 and 1905, or sent from
Japan to him at various times, I have had access to certain embryos of Chlamydoselachus
as follows. In the American Museum are six specimens ranging from 190 to 370 mm. in
length. In the zoological collection of Columbia University, and loaned to me by Prof.
J. H. McGregor, are 13 embryos of various sizes (but none so large as ours), some with
and some without yolk sacs; and five eggs without embryos; then in addition there are
four lots of embryos (mainly very young) collected in 1913, 1914 and 1917. Lastly from
the Museum of Comparative Zoology, Cambridge, Massachusetts, there have come
through the courtesy of Dr. Thomas Barbour, one small embryo brought from Japan in
1907; and an egg with a larger embryo presented by Dr. Dean in 1912.
THE DRAWINGS AND THEIR AUTHORSHIP
Found among Dean’s records are 55 finished drawings reproduced herein as plates
Ito VI. These drawings range from a representation of what is evidently an ovarian egg
to figures of specimens, male and female, in which the yolk sacs are no longer present. Of
the 55 drawings, three are in color and the others are in grey (pencil), but all were pre-
pared for reproduction by lithography. These figures were assembled on eleven unnum-
bered sheets of heavy cardboard, each plate comprising from one to nine figures. I could
not make out any graded arrangement of these drawings as afhxed to the sheets which
have come tome. With the help of Dr. B. G. Smith, I have endeavored to consolidate the
drawings of eggs and embryos and arrange them in sequence so far as is practicable—except
that the colored figures have been grouped on one plate. All the drawings of adults have
been grouped on the final plate.
The matter of the execution of the drawings, which form the basis for this article,
was at first a puzzle. It seemed probable that some of them were made by Dean, but
530 Bashford Dean Memorial Volume
there was reason to believe that most of them were done by Japanese artists under his
direction. No one, who is familiar with Dean’s skill as an artist, will doubt that he was
capable of making drawings like those reproduced in this article. But his time at Misaki
must have been fully occupied with pushing the collection and preparation not only of the
embryological material of his archaic fishes (particularly the more abundant eggs and em-
bryos of Heterodontus) but of the other rare zoological materials which he brought back to
Columbia University.
As will be shown later, Chlamydoselachus is an ovoviviparous shark. The embryos
with their huge yolk sacs, enclosed in egg capsules, were obtained from the uteri of the
female fish newly caught in Sagami Bay. Brought up from depths of from 300-600 fathoms,
these embryos presumably could not be kept alive in aquaria. They would be subjected to
two greatly changed conditions—a lower pressure and a higher temperature. Further,
there is probably a difference in the chemical composition of the surrounding medium
when eggs and embryos are transferred from the uterine fluid to sea water. However,
in the light of some personal observations, I cannot be sure of this. While a guest-in-
vestigator at the Tortugas (Florida) Station of the Carnegie Institution of Washington
(1912-15), I found that when the similar thick-shelled intra-oviducal eggs of the nurse
shark, Ginglymostoma cirratum (a shallow-water form), were removed from the uterus,
opened, and the perivitelline fluid tasted, this was found to be salt. It may be noted here
that the cloaca of the nurse shark has a wide external opening and that the common
opening into it of the two gravid uteri will often admit three or four fingers. A similar
testing of the perivitelline fluid of the uterine egg of a just-caught Chlamydoselachus
would be very instructive.
Even if the factor of chemical composition of the surrounding medium is ruled out,
still, because of the great alterations of pressure and temperature, the embryos of Chlamy-
doselachus would die quickly. Hence if they were to be drawn alive, the assistance of
several skilled artists would be required. In this connection and in corroboration of the
idea expressed above, Mrs. Dean states that she clearly remembers that Dr. Dean, while at
Misaki in 1900-1901, had the assistance of six artists and that on the second visit (1905)
he had four artists making drawings. Mrs. Dean is fortunately able from her diary to
give the names of the six artists—one of them being a man named Kuwabara.
Furthermore, Dean was, at the time of the collection of embryos of Chlamydoselachus,
also studying the much more abundant eggs and embryos of Heterodontus which were
comparatively easy to procure from shallow water with the aid of divers.
Since there are many drawings of the young stages of this shark, it is probable that
the artists devoted more time to these than to the embryos of Chlamydoselachus. Because
of the abundance of valuable Heterodontus material and because the less viable embry-
os of Chlamydoselachus must be preserved immediately, it seems probable that figures
of the embryos of the frilled shark were drawn at a later date from preserved specimens.
I surmise that the colored figures and probably some of the uncolored ones were made at
once from fresh specimens at Misaki, or that rough color sketches were made there, and
The Embryology of Chlamydoselachus 531
that later the finished sketches were made from these and from preserved specimens.
Finally, I have received from Dr. Naohide Yatsu, of Tokyo Imperial University,
information which confirms the conjectures above and adds further to our knowledge of
the authorship of these excellent drawings. Dr. Yatsu was associated with Dr. Dean
on the first visit to Japan, and afterwards at Columbia University, where he was a student
of Dean’s and later an assistant in the Department of Zoology.
On the matter in question, Yatsu writes that at Misaki, Dean made sketches in
pencil and in color from living embryos of Chlamydoselachus. Indeed among Dean’s
relicta is such a color sketch of the internal organs of a female Chlamydoselachus. As to
the finished drawings, Yatsu is sure that the color figures were made from Dean’s color
sketches and the pencil drawings from Dean’s sketches and also from preserved material.
These were done in Tokyo in 1905 under Dean’s supervision at the Zoological Institute of
the University by Isaburo Kuwabara, the Institute draftsman. This is also the testimony
of Yatsu’s colleague, Dr. Tanaka.
VIVIPARITY (OVOVIVIPARITY) IN CHLAMYDOSELACHUS
All elasmobranchs (sharks and rays), whether oviparous or viviparous, have internal
impregnation and fertilization. To effectuate this, the male is provided with intromittent
organs, the claspers. These are modified portions of the hinder and inner part of each
pelvic fin, which are inserted into the cloaca of the female and served to hold her fast and
to transmit the seminal fluid.
The preponderant evidence is that oviparity was the original method of reproduction
in elasmobranchs. It persists today in certain sharks and skates, which extrude eggs en-
closed in horny envelopes provided with tendrils by means of which they become at-
tached to marine objects. In Chlamydoselachus the large egg is enclosed in a keratinoid
capsule provided at each end with a process which varies greatly in form and structure.
It is sometimes blunt but in many instances it is long, curved, and frayed at the apex into
tendrils (Figures 2, 7 and 13, plate I). If these encapsuled eggs were found outside the
body of the fish, one would surmise that these curved processes serve as organs of attach-
ment. But egg and capsule are retained within the uterus even after the developing
embryo has burst the shell, as will be shown later.
Thus in this shark, the presence of the egg shell with curved horns or frayed pro-
cesses plainly indicates that the ancestors of Chlamydoselachus practiced oviparity. Yet in
the frilled shark, possessing so many primitive characters, there prevails the most highly
specialized form of reproduction—viviparity, or more properly ovoviviparity as will be
explained later. This is another instance of the strange admixture of primitive and
specialized characters found in Chlamydoselachus as pointed out by Smith in his study of
the anatomy (1937).
That the fish is viviparous must have been known to Ludwig Déderlein, who, in the
years 1879-1881, made an extensive collection of Japanese fishes. These were brought in
1881 to Vienna, and among them were two specimens of Chlamydoselachus taken in
532 Bashford Dean Memorial Volume
Tokyo Bay in 1881. At least one of these was a female. For the scanty history of these
two sharks see Gudger and Smith (1933, p. 248). As may be read therein, Doderlein
described the two specimens of Chlamydoselachus but his paper was lost. It is plain,
however, that he recognized that this shark is viviparous. For this see Rése’s statement
in a later paragraph in this section.
In 1884, the Museum of Comparative Zoology, Cambridge, Massachusetts, pur-
chased a slender snake-like shark from Prof. H. A. Ward, who had obtained it from Japan.
Samuel Garman, curator of fishes, seeing that it was a new form, at once published
preliminary descriptions of it and named it Chlamydoselachus anguineus (the snake-like
cloak-gilled shark). In 1885 Garman described the anatomy of this partially eviscerated
female specimen. He found the badly preserved ovaries and oviducts much torn, but of
Text-figure 2
A female Chlamydoselachus with the eggs which have been cut out of her body.
This figure has been carefully retouched to make the outlines clearer.
After Nishikawa, 1898, Fig., p. 95.
one of the oviducal tubes he says that “A piece left at the cloaca showed one of the [ovi]
ducts greatly distended, possible with young that had hatched within it”.
That this was a sound deduction is shown by Rése’s statement (1895, p. 194) that
“One of the animals [a female Chlamydoselachus brought from Japan by Doderlein] had
‘im Leibe’ an embryo about 340 mm. [13.4 in.] long, which Professor Déderlein had the
kindness to turn over to me for study”. With this statement of Rose’s, it became almost
certainly established that Chlamydoselachus brings forth its young alive.
However, the man who personally first definitely demonstrated that the frilled
shark is viviparous was the Japanese student, Nishikawa. In 1898, he wrote ““Chlamy-
doselachus anguineus is viviparous, and the breeding season is spring, extending from
about the end of March to the beginning of June”. Furthermore, he figured a female
shark and a number of eggs (Text-figure 2) taken from her body. This photograph was
poorly reproduced on soft paper and is without any explanatory legend. It is plain,
however, that these eggs are enormous in proportion to the size of the body of the fish.
The Embryology of Chlamydoselachus 533
It is impossible to determine with certainty how many eggs are represented in this
figure. There seem to be about a dozen and in addition there are various objects not
clearly recognizable. There is no date given for the capture of this fish, but from a female
taken May 26, 1896, Nishikawa obtained six embryos ranging from 32-60 mm. in length.
“Each embryo was attached to its large yolk-sac by means of an umbilical cord, which
allowed considerable movement to the embryo”.
Thus Nishikawa in 1898 was the first to demonstrate by dissection and publication
that Chlamydoselachus is viviparous. He had dissected seven specimens in 1896. Since
Dean kept closely in touch with the literature on the archaic fishes, it is likely that he
knew of Nishikawa’s article (1898) as is evidenced by his statement (Dean, 1901.1):
“I found... that if one could secure [at Misaki] many adult [female] specimens [of
Chlamydoselachus| there was a fair chance of obtaining embryos, since this shark was
known to be viviparous”’.
Dean’s extensive experience in collecting eggs and embryos at Misaki abundantly
confirmed the conclusion that Chlamydoselachus is viviparous. His stages ranged from
blastulae to embryos varying in length from 11.5 mm. to 390 mm. (15.35 in.)—all attached
to yolk sacs.
The spawning habits of the frilled shark are unknown to this day. It seems to me
that this fish must properly be called not viviparous but ovoviviparous, because it carries
in its uterus not eggs in very thin-walled capsules as do some viviparous sharks and rays,
but eggs with rather heavy keratinoid shells fit to be expelled into the water (Figures 2
to 10, plate I).
I have found that the tropical littoral nurse shark, Ginglymostoma cirratum, carries
in its uteri very large eggs enclosed in very heavy keratinoid shells. Evidence (to be
adduced later) leads to the belief that, when the embryo has attained some size the shell is
burst and is expelled through the cloaca into the sea, while the egg and embryo are re-
tained in the uterus for a considerable time For these reasons, it seems to me that such
a shark ought to be designated as ovoviviparous rather than viviparous. I have studied
the nurse shark extensively and since its reproductive organs and breeding habits are very
similar to those of the frilled shark, comparisons will frequently be made in order to clear
up many puzzling questions about the reproduction of Chlamydoselachus.
The young frilled shark certainly breaks its egg shell long before it is old enough to
be extruded from the uterus into the water (Figure 11, plate I). But we do not know at
what stage in the development of the embryo the insoluble keratinoid egg capsule is cast
off into the uterus nor when it is extruded into the sea. Nor is it known whether the
embryo is expelled into the water before all the yolk is absorbed as occurs in the dogfish,
but is seems improbable. If the young Chlamydoselachus or Ginglymostoma were extrud-
ed early, it would swim poorly because of its great yolk mass (Figure 49, plate V) and
would be an easy prey for any marauding fish. One must conjecture that the young of
both sharks are retained in the uterus until, when passed out into the sea, they are able
534 Bashford Dean Memorial Volume
to fend for themselves. In support of this I have found (Gudger, 1918) that the 20-mm.
eggs of the marine gaff-topsail catfish (Felichthys felis), which are orally incubated, are
retained in the mouth of the male not only until the egg shell is thrown off but until all
the large yolk mass is taken into the body of the young fish. Thus the little three- or
four-inch fish when set free in the ocean is better equipped to escape its enemies and
capture its food.
BREEDING SEASON OF THE FRILLED SHARK
Because of its deep-sea habitat, no direct observations on the breeding behavior and
season of this shark have ever been made. Consequently we are confined toa study of the
records indicating the stages of development of ovarian eggs and of uterine embryos on
the dates of capture of the females. The evidence from the ovaries, since it does not
include accounts of eggs ready to be discharged, is not of great value. Of prime im-
portance, however, are the data as to stages of development of embryos in the oviducts.
The all too scanty evidence from both sources will now be presented.
EVIDENCE FROM THE OVARIES
With one exception, the only available evidence from this source as to the breeding
season of Chlamydoselachus is contained in the entries in Dean’s notebook concerning eggs
found in these organs. These fragmentary statements, being dated, do throw some light
on the matter.
Text-figure 3
The partially opened abdomen of a 1510-mm. female frilled shark taken November 28, 1938,
in the Sagami Sea. Five eggs, each measuring 80—83 mm., were contained in each ovary.
: Photograph by courtesy of Fumio Momose.
The Embryology of Chlamydoselachus 535
In the handwriting of Dean’s unnamed Japanese collector—possibly Kuma—are two
records. In the ovary of a 1500mm. Chlamydoselachus taken February 8, 1905, six
‘immature’ eggs were found. And on April 30, 1903, he found in a female, 1670 mm. in
length, three “immature” eggs in one ovary and nine in the other. Unfortunately the
sizes of these eggs were not noted. However, under date of April 27 (1902?), Dean
diagrammatically figured and also photographed the ovaries with eleven large eggs in
a female measuring 1960 mm.—the largest Chlamydoselachus on record. In the left ovary
were five eggs, size 70 x 30 mm., and in the right nine of the same size and two measuring
60 x 30mm. As will be seen later, these eggs, though large, were not mature, but one
may conjecture that they would have reached maturity later in the calendar year. Thus
Dean recorded on October 1, 1905, “female, no eggs [in oviducts ?], large ovar.”
Since the above was written, Momose (1938) has described the visceral anatomy of
a nearly ripe female taken in Sagami Bay, November 28, 1938. Each ovary contained five
eggs measuring from 80 to 83 mm. in diameter. Momose has kindly sent me two photo-
graphs showing this fish opened along the mid-ventral line to reveal the ovaries. The
better of these photographs is reproduced herein as Text-figure 3. Since ripe ovarian eggs
and newly fertilized eggs (Figures 1, and 4, plate I) average about 95 mm. in diameter, it
is clear that these 80-83-mm. eggs were almost mature.
The evidence from the ovaries is scanty but nevertheless significant. To recapitulate,
ovarian eggs taken February 8 and April 30 were noted as “immature” but no sizes were
recorded. However, on April 27 some eggs were measured and found to be 70 x 30 mm.
On October 1 a “large ovar.’’ was noted, and on November 28, several eggs measuring
about 83 x 80 mm. were photographed (Text-figure 3)—-eggs almost “ripe”. These data
indicate strongly that eggs in the ovaries of Chlamydoselachus ripen at any season through
out the year. But better evidence of a long breeding season will now be introduced.
STAGES OF EMBRYOS IN THE UTERI
The evidence as to the surprising range of the breeding season of the frilled shark,
based on the ages of embryos obtained from the uteri, at various times in the year, will
now be set out in chronological order.
Nishikawa (1898) gives the first intimation of a definite breeding season for the frilled
shark. He states that **. . . the breeding season is spring, extending from about the end of
March to the beginning of June”. He had eggs in early and late blastula stages but he
does not give the dates when these were obtained. Of his seven gravid female fish,
he gives date of collection for but one. His youngest batch of embryos (from a 1700-mm.
female) came to him on May 26, 1896. These embryos were six in number and measured
32, 35, 43, 48, 50 and 60 mm. long respectively.
Dean’s notes give a far greater range of dates when uterine eggs and embryos were
collected, and ordinarily he gives measurements for one or both. Thus he notes “1905,
Early Jan. [not June] eggs with embryos 11.5, 15.5, and 20 mm.” Furthermore, in the
jar of material from Columbia University referred to above there are two embryos of
536 Bashford Dean Memorial Volume
about 20 and 45 mm. in length, without yolk sacs, bought in the Tokyo market January 22,
1914. These and other embryos from this jar are badly crumpled, hence the “about” for
this and the three other lots. In this same jar are four embryos about 15, 18, 20 and 25 mm.
“over all”, “from Tokyo market February 4, 1913”. In the same receptacle are seven
embryos ranging from about 60-130 mm. in length “Bought Tokyo Market April 4,
1913°. In his notebook Dean states that he got three blastulae on April 10 (year not
noted). Next and last of the four Columbia University lots are five embryos measuring
about 23, 25, 30, 43 and 47 mm. bought on April 23, 1917.
The remainder of the available data is also from Dean’s notebook. On April 25 he
records seven eggs with embryos—165, 175, 185, 195, 205, 210 and 250 mm. in length.
Then in the writing of his unknown note-taker and correspondent, judged to bea Japanese,
are recorded eggs from the oviducts of three females each measuring 1770 mm. The
first taken April 25 had seven eggs with embryos (not measured), the second (of the same
date) had five “broken eggs” in the oviduct; the third, taken April 27, had in the oviduct
three “mature” eggs (two broken). Next in Dean’s writing is this record “4 embs. large,
taken about May 1, 1905”. These measured in millimeters 317, 331 (yolk sac 111 x 100),
352, 390 (yolk 100 x 70). Then I find in Dean’s writing a record, *? May 23, 1906,” of five
embryos (no measurements) from a 1390-mm. female. The next records come from late in
the calendar year and are so important that they must be given in a separate paragraph.
Four eggs were taken from the uteri of a female captured in the Odowara Bank on or
about October 1, 1905. This record is based on three separate notes in Dean’s writing on
three separate pages of his notebook. No one of these, no two would establish this fact;
but when all three are studied together, date, place, and number of eggs all tie up into
this definite record. Three of these eggs are noted as “oblong eggs, 2 drawn, in r. oviduct,
small wind egg (drawn) in opposite [I.] oviduct, stage early [small pencil sketch] probably
gastrula”. For the two “oblong eggs”, see Figures 2 and 3, plate I. Apparently the
oblong egg with the probable gastrula, shown in the pencil sketch (Text-figure 26), was
not drawn. For the “small wind egg” see Figure 51, plate V.
Among Dean’s loose papers, I have found a rough sketch in water color of an egg and
embryo labelled (in a hand other than Dean’s) “Chlamydoselachus anguineus. Egg taken
at out of Okinose, Sagami Sea. (Depth 360 fms.) December "06". The egg and embryo
were presumably drawn natural size. The ellipsoidal yolk measured 122 x 69 mm., and the
embryo 55 mm.—when taken in December!
Here let us recapitulate the dates throughout the whole calendar year on which
embryos of the sizes noted have been taken: “Early Jan.”, six specimens measuring 11.5
to 20 mm.; April 4, seven—60 to 130 mm.; April 10, three blastulae; April 23, five
embryos—23 to 47 mm.; April 25, seven, 165 to 250 mm.; April 25 and April 27, fifteen
eggs and embryos in three uteri; May 1, four embryos—317 to 390 mm.; May 23, five—no
measurements: October 1, three eggs—probably blastulae; December 06, one embryo
55 mm.—in length.
The Embryology of Chlamydoselachus 537
The evidence from the ovaries is fairly strong, that from the uteri cumulative and
overwhelming, that Chlamydoselachus ripens eggs in batches in its ovaries, and broods
and hatches embryos in its uteri throughout the whole calendar year and probably in
every month of the year.
When one thinks the matter out, this does not seem so extraordinary as at first blush.
Chlamydoselachus lives at the bottom of the Sagami Sea under uniform conditions of
darkness, great pressure, low temperature, with a restricted oxygen supply, and on food
with presumably little change in kind and quality. The maximum depth of the habitat of
the frilled shark is about 3600 feet, the average 1500 to 1800. At 1800 feet the pressure is
814 lbs. to the square inch, the temperature about 43° F. and the human eye would find
total darkness. Under the prevailing and unvarying conditions at these depths, the
frilled shark would presumably have no special breeding season such as is found in surface-
dwelling sharks in the Sagami Sea. In these, in contrast, breeding might be expected
to take place in late spring or early summer due to the lengthening daylight period, the
rising temperature, and the more abundant food consequent upon the return of the sun.
In Chlamydoselachus, on the contrary, it is to be expected that eggs would ripen in the
ovaries at any time during the year as indicated above and that breeding would take place
during any month. Thus the findings of eggs with blastulae in October and of embryos
10-20 mm. long in January, and others measuring 317-390 mm. in May—as recorded by
Dean—are understandable.
Before leaving this subject, it is pertinent to call attention to the notes above, which
show that not all the eggs in a single uterus are in precisely the same stage of development.
Even as the eggs break out of the ovary one at time as they ripen, so they make their way
into the oviduct one at a time. Hence there must be a continuous process of fertilization,
shell formation, and early development going on within a single female during a limited
period of time. This I have found to take place in the shallow-water nurse shark of Florida.
Likewise, there will be much later, in the uterus of each individual female Chlamydo-
selachus, a serial process of breaking and throwing off of egg capsules by the growing
embryos, and finally a succession of young sharks being extruded into the sea.
It should be noted that ovarian eggs are matured in batches or clutches (a small
number of approximately the same large size) and that, when nearly mature eggs are
present in the ovary, there are no other eggs in the ovaries of the same individual at all
comparable in size. Also, there are limits to the range of variation in sizes of embryos
obtained from a single female at the same time. One does not find very early and very
late embryos developing in a single individual at the same time. These observations indi-
cate that in each individual Chlamydoselachus there is a definite cycle of reproductive
activity, but one quite independent of seasonal influences, hence any single phase of re-
production and development may occur in different individuals at different seasons of the
year. In this, Chlamydoselachus is unlike most vertebrates, but a comparable condition
is found in civilized man.
538 Bashford Dean Memorial Volume
DURATION OF GESTATION
The duration of the period of gestation in the frilled shark is not known, and, because
of the habitat of the breeding fish and of the absence of any definite breeding season, it
cannot be ascertained by direct observation. However, it will be of interest to set forth
some facts that indicate that the period is protracted. The same factors of constant low
temperature, great pressure, and restricted oxygen supply, that lead to an extension of the
breeding season to cover the calendar year, would also be conducive to slow development
of the embryos and a lengthened period of gestation.
Textfigure 4
Egg shell (measuring 128 mm.), egg (100 x 65 mm.), and embryo (43 mm.) of Chlamydo-
selachus, reproduced in natural size.
After Nishikawa, 1898, Fig. 1, pl. IV.
An idea of the duration of this period may be gained by studying a series of growing
embryos and noting the relative diminution of their yolk sacs. But first one must endeavor
to establish the normal size of the yolk mass at, or shortly following fertilization. The
matter of the varying sizes of the eggs of Chlamydoselachus will be taken up later. Here
we are interested in the size of the eggs in blastula or gastrula stages or in early stages
of embryonic development. Only two investigators have studied such eggs. The first of
these, Nishikawa (1898), states that the eggs (in early stages of development, probably
segmentation), range from 65 to 75 mm. in short and from 102 to 124 mm. in long diameter.
He writes of other eggs ranging from 110 to 120 mm. in long diameter. These measure-
ments are probably made over the egg shell. Thus Text-figure 4 (his Fig. 1, tab. IV)
is 128 mm. long in a straight line over the horns of the shell, whereas the egg itself
measures 100 x 65 mm., and the embryo 43 mm. in length. The egg shown in Text-figure 4
is in natural size.
The Embryology of Chlamydoselachus 539
Dean portrays three eggs in blastula or gastrula stages in Figures 4, 5, and 6, plate I.
The yolks measure: A, 97 x 88 mm.; B, 96 x 87; C, 90 x 87. Of eggs and early embryos in
stages of development comparable to Nishikawa’s 43-mm. embryo, Dean had three drawn.
Figure 7, plate I shows a yolk 100 x 65 mm. with an embryo of 43 mm.; (as will be seen
later, this isa copy of Nishikawa’s Fig. 1, plate IV); in Figure 9, plate I, the yolk measures
108 x 68, the embryo 50 mm.; and lastly there is the drawing in color, Figure 50, plate V,
with a yolk 95 x 69 and an embryo of 39 mm. In these early stages there is practically no
diminution of yolk size.
To illustrate the slow rate of absorption of yolk, we may consider three large embryos
listed by Dean. Thus in Figure 11, plate I, an embryo of 175 mm. (magnified to 205 mm.)
sits on a yolk measuring 92x 89mm. This was collected April 25. Then “taken about
May 1, 1905” were two still larger embryos. The smaller measured 331 mm. in length
and had a huge yolk sac measuring 110 x 100 mm. The other is the largest embryo of
which there is record. This fish, shown in color in Figure 49, plate V, was 390 mm.
(15.35 in.) long and its yolk sac was 100 x '70 mm. in its transverse diameters.
To recapitulate, Dean’s notes will be quoted. The specimens of Oct. 1, 1905,
“stage early, probably gastrula”, might possibly have grown by “early January” into
embryos measuring 11.5, 15.5, and 20 mm. on yolk sacs undiminished in size. But it
does not seem likely that by “Apr. 25” one of these could have attained the size of the
175-mm. embryo of Figure 11, plate I. Nor could the 175-mm. fishlet by ““May 1” have
grown toan embryo of 390 mm. (yolk 100 x 70), which is represented in Figure 49, plate V.
From the above data it is clear that the fish grows much faster than the yolk decreases.
It is evident that all the yolk must be resorbed before the little shark is thrown out.
into the sea to fend for itself. The 15.35-in. fish portrayed in Figure 49, plate V, would be
so encumbered in swimming, and the large yolk covered with blood vessels would be so
conspicuous and attractive to marauders, that the free life span of the fish would probably
be but a few hours at most. But how large would the young shark be when it has used up
all the food yolk? Surely it would be much larger—perhaps 20-24 in. (508-610 mm.)
long. The latter size is that of a free-swimming Chlamydoselachus taken by the Prince
of Monaco at Madeira (Collett, 1910). But would the uterus of the average-sized female
contain such a large “baby” without its being folded or curled up? And could it contain
several embryos of this size?
All the evidence points to a very long period of gestation in Chlamydoselachus. But
how long? Because of its habitat and its breeding throughout the year, it is of course
impossible to find the answer in the body or in the habits of the frilled shark. It is
practically impossible to ascertain the length of time for the hatching of any shark’s egg
save in the oviparous forms—and only in those species small enough to be kept in aquaria,
where the date of egg-extrusion and of egg-hatching can be recorded. This has been done
in terms of “about so many days” for two species of dogfish. One must say “about” for
one cannot know how far in development an internally-fertilized oviparous egg has gone
when it is “laid”. Here are all the facts, so far as known to me.
540 Bashford Dean Memorial Volume
As early as 1867, Coste described how a pair of spotted dogfish, Squalus (Scyllium ?)
catulus were introduced into the vivarium at Concarneau (a rock-encircled arm of the sea
shut off by gratings). The female extruded 18 eggs during the month of April, and the
young were hatched out during the month of December. Thus the period between
laying and hatching was about 8 months—not “about 9” as stated by Coste.
Bolau (1881) is more exact. On April 12, 1877, the Hamburg Aquarium received
from the Brighton Aquarium a number of eggs of the European dogfish, Scyllium canicula,
(how long after extrusion is not stated). Four of these hatched as follows—December 3,
1877, and January 1, 4, 17, 1878. Their periods were 235, 264, 267, 280 days—from 7
months and 21 days to 9 months and 10 days. Seven eggs of the catshark, Scyllium
catulus (also from Brighton), hatched from August 19 to October 16—a time space of
129-187 days or 4 months and 9 days to 6 months 7 days. That same season an egg laid
in the aquarium hatched in 180 days. During 1878 a number of catshark eggs were de-
posited in the same aquarium and 10 of them hatched in periods varying from 157 to 178
days or from 5 months and 7 days to 5 months and 28 days.
These are the known facts, but more data are needed. In comparison there is reason
to believe that, while incubation is going on, the female frilled shark is living in water of
probably not over 43°F. (at a depth of 1800 feet.). But what were the ranges of tempera-
ture to which the dogfish eggs were exposed at Concarneau and at Hamburg? We have
already noted the great size of the egg of Chlamydoselachus. Bolau tells us that the barrow-
or stretcher-shaped eggs of Scyllium canicula were 110 mm. long (over the horns) by
41 mm. broad (over the case). The corresponding measurements of the similar eggs of
S. catulus are 60-55 mm. long by 24-22 wide. The sizes of the yolk masses in these eggs
are not given, but they are undoubtedly far smaller than those of Chlamydoselachus—
probably not more than one-third to one-fourth as large.
If it takes these relatively small eggs of the European dogfishes from 5.5 to 9.5
months to hatch at the spring, summer and autumn temperatures of the English Channel
and the North Sea, how much longer must it take for the huge eggs of the frilled shark to
hatch at the uniformly low temperatures of 1800 to 3600 feet down in the Sagami Sea?
At first I was inclined to think that the incubation period lasted at least one year. But
since Kyle (Biology of Fishes, p. 66) says that the embryo of Acanthias takes about a year
to develop, it seems probable that it will take at least two years for the embryo of Chlamy-
doselachus to attain its full development.
It is unfortunate that Dean did not get large frilled-shark embryos later than May 1,
and larger than the longest of that date (390 mm., yolk 100 x 70 mm.), with yolks either
gone or nearing resorption. Such data would be of great value not only for the question
under consideration, but for giving an idea of the amount of distention of the uterus “at
term”, and as indicating the size of the young shark at the time of birth. It is also unfortu-
nate that no young free-swimming sharks were taken in the intensive deep-sea hook-
trawl fishing carried on in the Sagami Sea by Kuma and the market fishermen. The
smallest free-swimming specimen (a female) recorded by Dean measured 1240 mm. (48.8
The Embryology of Chlamydoselachus 541
in.), and the smallest ever put on record was taken by the Prince of Monaco at Funchal,
Madeira, in 1889. Collett (1890) found this to be a female only 610 mm. (24 in.) long.
He notes that it differed from typical adults from Japan only in insignificant details. He
gives no figure.
THE REPRODUCTIVE ORGANS OF THE MALE
CHLAMYDOSELACHUS
In general, the internal reproductive organs of the male frilled shark are like those of
the other elasmobranchs. They have been figured and described by Smith in the preced-
ing article of this volume. Here it is necessary to present only a brief account of the
external organs of reproduction in the male.
MYXOPTERYGIA—EXTERNAL ORGANS OF THE MALE
The male shark has the curious intromittent organs, peculiar to the elasmobranchs,
called the myxopterygia or claspers. They are modifications of the hinder inner parts of
the pelvic fins of the male shark or ray. These secondary sex organs, as Text-figure 5
Text-figure 5.
A 1500-mm. (?) male frilled shark from the Odowara Bank,
Sea of Sagami, Japan. Note the large myxopterygia or claspers.
These are developed from the inner parts of the pelvic fins.
The claspers help the male shark to hold the female during
copulation.
After Doflein, 1906, p. 257.
Text-figure 6
Ventral view of the pelvic region of a male Chlamydoselachus,
showing myxopterygia or claspers. Through the tubular
claspers, the seminal fluid is introduced into the cloaca of the
female. This is necessary since in all sharks impregnation of
the eggs is internal. The cloacal aperture may be seen be-
tween the bases of the myxopterygia.
Cav., projection of cavity.
After Leigh-Sharpe, 1926, Fig. 1, p. 308.
542 Bashford Dean Memorial Volume
shows, enable one at a glance to distinguish the male. The claspers are necessary because
impregnation in all sharks is internal. These myxopterygia are the only reproductive
structures of the male that we need consider here. For elasmobranchs in general, they
have been admirably described by Leigh-Sharpe, (1920, p. 245) from whose article I quote
the following:
. .. the basal element of each pelvic fin (basipterygium) is prolonged to form a stout
backwardly directed skeletal rod supporting a portion of the fin which is demarcated from
the remainder and specially modified to form a copulatory organ, the clasper or myxopter-
ygium .. . The clasper is rolled up in a manner resembling a scroll | Text-figure 6] so that in-
stead of being a groove, as it is usually described, it is a sufficiently closed tube along the
greater portion of its length, though the edges may not be and usually are not completely
fused but overlapping. This tube is one along which spermatozoa pass.
Not only do the claspers serve as intromittent organs, but inserted into the cloaca
of a female they help hold her fast during copulation. Their appearance in lateral view of
a male Chlamydoselachus is shown in Text-figure 5 and of another in Figure 53, plate VI.
In Text-figure 6, we see these rolled-up organs in ventral aspect with the cloaca between
their bases. No further description is necessary here.
Text-figure 7
A 1510-mm. female Chlamydoselachus, whose enlarged abdomen is due to the presence in her ovaries
of 10 eggs measuring 80—83 mm. in diameter, as seen in Text-figures 3 and 9. Note the absence of
any external secondary sex characters.
Photograph by courtesy of Fumio Momose.
REPRODUCTIVE ORGANS OF THE FEMALE
CHLAMYDOSELACHUS
The female frilled shark (Text-figure 7) has no external secondary sex characters, but
when the ovarian eggs approach ripeness or particularly when the uteri are filled with
huge eggs undergoing development, the distended abdomen indicates pretty clearly the
sex of the fish even though the pelvic fins are not distinctly visible. Thus all the repro-
ductive organs of the female, the ovaries and the oviducts(with their various subdivisions),
are internal. They have been thoroughly described by Smith (1937) in the article dealing
with the anatomy of Chlamydoselachus, but it will be necessary to consider here certain
features having to do with viviparous reproduction in this fish. These are: first, the
enormous size attained by the eggs while still in the ovary; second, the great distention
The Embryology of Chlamydoselachus 543
of the uterine portion of the right, and rarely the left oviduct, which is necessary to ac-
commodate the huge eggs and later the yolk sacs and the developing embryos in this
viviparous shark.
In going through Dr. Dean’s few scattered notes—literally with a magnifying glass
because they are at times written in a minute hand—I have been able to correlate certain
widely separated records and to find certain data either overlooked or not clearly evaluated
before. These have to do mainly with the reproductive organs of the female and with the
question as to whether those of both sides are functional or whether those of only one
side are used in reproduction. These data are so interesting and so valuable that they
deserve careful study. However, we will first take up the literature dealing with each
set of organs—ovaries and oviducts—and then consider Dean’s notes which will throw
much light on both structure and function.
Text-figure 8
Ovaries and oviducts of Chlamydoselachus, drawn one-half natural size.
n. g., nidamental glands.
Printed from the original woodcut after the drawing by Paulus Roetter for Garman, 1885, Fig. 1, pl. XIX.
The ovaries and the anterior portions of the oviducts of Chlamydoselachus were
first figured by Garman (1885). Because of its historic interest, his drawing is reproduced
from the original woodcut (Text-figure 8 herein). Garman merely says of these organs
“A section some 12 inches in length of the ovaries and oviducts is represented in the
sketch”. It isa long jump from Garman’s figure (1885) to Deinega’s representation (1925)
of the genital organs of our fish. His small figure printed on poor paper is not easy to
understand. However, Smith’s admirable drawings, made from his dissections of four
specimens from Japan in the Museum collection, give a clear picture of the form and the
relative sizes of the female reproductive organs in various stages of development. They
will be referred to later for positions and structures of both ovaries and oviducts.
And last of all Momose (1938) has figured the abdominal viscera of a 1510-mm.
female Chlamydoselachus with the huge ovaries removed. This figure is reproduced in
his article in small size on soft paper and is not suitable for reproduction. However,
Momose has been good enough to send me the original drawing with the huge ovaries
544 Bashford Dean Memorial Volume
(with their 10 eggs, each measuring 80-83 mm. in diameter) sketched in. This is re-
produced herein as Text-figure 9. Being labelled, it needs no explanation here beyond the
remark that the non-gravid uteri are of approximately the same size.
Text-figure 9
Semi-diagrammatic sketch to show the repro-
ductive organs of a 1510-mm. female Chlamydosel-
achus. Note the five huge eggs (80—83 mm.) in
each ovary, and the paired oviducts with their
subdivisions. One shell gland is opened to show
its structure, and both uteri are somewhat
dilated.
Sketch by courtesy of F. Momose.
THE OVARIES
In Chlamydoselachus, the ovaries are paired,
elongate, and in the non-breeding female,
more or less flattened organs situated in the
anterior part of the body cavity and attached,
rather indirectly, to the dorsal body wall by
means of broad mesenteries. These organs
like others in this fish are subject to some
interesting variations which will be pointed
out further on.
Before Smith’s studies (1937), but three in-
vestigators had published observations on the
ovaries of Chlamydoselachus. Garman (1885)
merely remarks—“The ovaries [Text-figure 8]
had been badly preserved and were much
torn”. Collett (1897) describes the oviducts
and then continues as follows: “The right
uterus [ovary?] was 240 mm. in length, and
contained 10 large eggs about the size of the
yolk of a small hen’s egg, but some varied in
size. There were, besides, about 30 lesser
yolks of the size of large and small peas, as
well as a few bigger ones about the size of the
yolk of a pigeon’s egg. The length of the left
uterus [ovary] was 220 mm., and it contained
five large yolks, and about 20 small ones.”
This is understandable only on the sup-
position that Collett used the word “uterus”
but meant ovary. In the paragraph preceding
the one quoted, he crudely described the
oviducts—stating that they were 900 mm.
long and that each expanded into “a uterus-
like sack”. His description of the “uterus” in
the above quotation, if “uterus” is replaced
by ovary, absolutely fits the structure of the
immature elasmobranch ovary having in it
The Embryology of Chlamydoselachus 545
eggs of various sizes and of various degrees of “ripeness” such as I have found in the
ovaries in scores of dissected sharks and rays. Furthermore, although, as I have found, all
the eggs in the uterus of a viviparous shark or ray may vary somewhat in size, the limits
are fairly close. They do not vary from “the size of the yolk of a small hen’s egg” to that
“of large and small peas”. Then too when a wind egg is found, it, though smaller in size,
Urogenital system of the female Chlamydosel-
achus, ventral views, one-fifth natural size.
Text-figure 10. Urogenital organs of a specimen
1398 mm. long. The excretory ducts are
concealed by the oviducts.
ab.p., abdominal pore; m, mesonephros; ovd., oviduct; ovy.,
ovary; r.cl., rectal portion of the cloaca; ug.s., opening from
the urogenital sinus; v.I., ventral ligament of the oviduct.
Drawn from specimen No. IV in the American Museum
of Natural History.
After Smith, 1937, p. 432.
Text-figure 11. Urogenital organs of a specimen
1550 mm. long. The shell glands and the
adjacent portions of the oviducts are displaced
laterally, and the excretory ducts are not shown.
ab.p., abdominal pore; m., mesonephros; ovd., oviduct;
ovy., ovary; r.cl., rectal portion of the cloaca; s.g., shell
gland; ur.p., urethral pore; ut., uterus; v.I., ventral ligament
of the oviduct.
Drawn from specimen No. III in the American Museum
of Natural History.
After Smith, 1937, p. 432.
Text-figure 10. Text-figure 11.
is plainly recognizable as being a shell without embryo and yolk. To settle the matter
effectively, attention is called to the fact that Collett does not speak of egg shells. He
wrote uterus but he surely meant ovary.
It seems that this misidentification of the genital organs may be due to the possibility
that Collett wrote in Norwegian and that his thesis was translated into English by another
hand and that it was published without his seeing the proofs.
Hawkes (1907) had several specimens, but, of the organs under consideration, she
briefly states that ‘“The ovaries are diffuse bodies attached by broad mesenteries to the
546 Bashford Dean Memorial Volume
line of attachment of the stomach mesentery”. From this, one may judge that her spec-
imens were either immature or with ovaries spent. Deinega’s specimen (1925) had had
the ovaries removed. Smith (1937), however, gives definite data, particularly in that he
records the sizes of eggs found in the ovaries of two of his fish. Unfortunatley, there are
no dates of capture of any of his specimens.
Ina sexually immature female specimen, 1398 mm. long (Text-figure 10), Smith found
that the ovaries were small and exhibited perfect bilateral symmetry. The largest fol-
licles measured only 10 mm. in their greatest diameter. In a larger and nearly mature fish,
1550 mm. long, he found that both ovaries were well developed and contained follicles
ranging in size up to 17 mm. in diameter as shown in Text-figure 11. Of the follicles large
enough to be easily distinguished macroscopically, there were 13 on the left and 15 on the
right. Some of those in the left ovary were larger than any in the right organ. In sexually
mature specimens, 1350 and 1485 mm. long respectively, he found the ovaries of the right
sides were spent and that those of the left sides were intact but small and contained only
very small ovocytes, none more than 6 mm. in diameter (Text-figures 14 and 15).
In Dean’s notebook on a pasted-in sheet (from its phraseology evidently from one of
his Japanese collectors) are two records concerning the ovaries. The first is dated
February 8, 1905, and reads “Six immature eggs in left ovary” of a 1500-mm. female.
Under date of April 30, 1903, this entry occurs: “Three immature eggs were in the left
ovary and nine immature eggs were in the right ovary” of a female 1670 mm. long. How
large these eggs were cannot be stated, but at least they were of considerable size. Never-
theless, for another fish, we do have measurements of the eggs.
There is in this same notebook a rough pencil sketch and some notes in Dean’s own
writing, showing that on April 27th he dissected a 1960-mm. female (the largest Chlamy-
doselachus on record). This fish had in the right ovary 11 eggs in two rows (nine measur-
ing 70 x 30 mm. and two 60 x 30 mm.), and 5 (70 x 30 mm.) in the left ovary. These large
eggs are found on the margin of the genital fold precisely as they are shown in Text-figure
11 (Smith’s 1550-mm. specimen), and as I have found them in mature ovaries in sharks of
southern Florida. These eggs were surely approaching maturity.
Among Dean’s Chlamydoselachus records is a faded photograph of the viscera of this
same female. This shows the 5 large eggs on the left side, but on the right only 6 or 7
can be counted—the precise number is uncertain because some are covered by the other
viscera. Lastly there is an incomplete water-color sketch of this same dissected fish. The
photograph and the color sketch were evidently intended to furnish the basis for a finished
figure in color. This, unfortunately, was either never made or has been lost. Dean’s
photograph is faded and the ovaries with their eggs are too much obscured by other
viscera to permit its use. The wash drawing and pencil sketch are plainly unfinished.
But fortunately other photographs are at hand to show these organs.
Momose in 1938 procured from Sagami Bay a 1510-mm. female having 10 nearly
ripe eggs (size 80-83 mm.) in the ovaries—5 on each side. His figure is poorly printed on
soft paper and is not suitable for reproduction. But, in answer to a request conveyed
The Embryology of Chlamydoselachus 547
through Dr. N. Yatsu, he has sent me two photographs showing the body cavity open-
ed along the mid-ventral line. The better of the photographs, and the one which he re-
produced, is shown herein as Text-figure 3. Momose also kindly sent me his drawing of
the abdominal viscera of his Chlamydoselachus with the two huge ovaries sketched in, as
seen in Text-figure 9. Each ovary contains five great eggs, measuring 80-83 mm. in di-
ameter. It is interesting to find in Momose’s photograph (Text-figure 3) and sketch
(Text-figure 9) absolute corroboration of what is seen in Dean’s 35-year-old photograph, in
his rough colored wash drawing, and in his rougher pencil sketch.
So far as all this evidence goes, it strongly indicates that more eggs ripen in the right
than in the left ovary—a total of 25 in the right and 19 in the left ovary in the four cases
cited above. In Dean’s specimen, having 5 eggs in the left and 11 (in two rows) in the
right, and in Momose’s fish having 5 eggs in each ovary are found the only cases on record
in which the left ovary contained eggs approaching maturity. Smith’s 1550-mm. specimen
contained young eggs in both ovaries, but the larger ovocytes (up to 17 mm. in diameter)
were found in the left ovary. Even with these bilateral ovaries considered, the weight of
evidence is that the right ovary is the predominant egg-producer.
It is interesting to note the relative positions of the ovaries with regard to each other.
Garman’s drawing (1885) shows the two ovaries on the same level (Text-figure 8 herein).
Hawkes (1907) says of her specimens (number not noted) that “The right ovary is placed
somewhat more anteriorly than the left”. Dean’s rough sketch shows the two organs on
the same level. Smith’s young and sexually immature fish (1398 mm. long) had the two
ovaries on the same level (Text-figure 10 herein). Another, measuring 1550 mm. with
eggs up to 17 mm. in the left ovary, had this ovary somewhat further forward than the
right (Text-figure 11). In each of his two other mature specimens (1350 and 1585 mm.
long) the right ovary was placed markedly forward of the left (Text-figures 14 and 15).
Momose’s sketch shows the relative positions of the ovaries in his specimen. The right
ovary is placed forward of the left by about two-thirds the diameter of one of the huge
eggs (Text-figure 9).
Of the eight females for which we have data, three had the ovaries on the same level
(one being sexually immature), one had the left anterior to the right, and four had the
right placed further forward. This difference in position brings the right ovary nearer to
the entrance funnel to the oviducts.
The matter of the one-sidedness of elasmobranchs in their reproductive organs—
particularly that in Chlamydoselachus the right ovary only tends to be functional—is of
very great interest and deserves some study. Fortunately I have made some firsthand
observations as to unilaterality of the functioning of both ovaries and oviducts in various
sharks and rays. It seems best to postpone the consideration of these data for ovaries
until the oviducts of Chlamydoselachus have been studied, since in them also a tendency to
unilaterality will be found, and since the functioning of the two are interdependent. But
before going into the matter of oviducts, it seems well to consider here the question of the
size attained by the egg before it is discharged from the ovary.
548 Bashford Dean Memorial Volume
IMMATURE OVARIAN EGGS
Among the frilled-shark material loaned by the Department of Zoology of Columbia
University are five ovarian eggs of different sizes. No. 1 (42 x 34 x 34 mm.) is greatly
flattened on one side and is devoid of follicular membranes. No. 2 (45 x 38 x 38 mm.)
is shaped like a hen’s egg and is surrounded with fragments of the follicular membranes.
No. 3 (46 x 46 x 35 mm.) is without follicular membranes. No. 4 (58 x 50 x 44 mm.) is
enclosed in follicular mem-
branes. No. 5—also enclosed
in follicular membranes—
measures 60 x 49 x 49 mm.
These are all immature eggs,
probably about half-grown.
Other sizable (and in this
case larger) ovarian eggs are
those noted and sketched by
Dean and taken from his huge’
1960-mm. sharkcaptured April
27. Of the 16 eggs in question
in the two ovaries, 14 measur-
ed 70 x 30 mm. and 2 were
60x 30mm. They approached
maturity much more than the
smaller eggs just listed above.
Last of all are the huge ovarian
eggs reported by Momose
(1938) from his 1510-mm. speci
Text-figure 12 men taken November 28.
A ripe ovarian egg in its ovarian and follicular membranes. The These, measuring 80-83 mm.
circular area on top is probably a thin place in the membranes where i diameter (Text-figures 3
the follicle will rupture to set the egg free into the coelom. This is
probably the same egg as that shown in Figure 1, plate I. It is and 9), were tea as
presumably figured in natural size. will be seen from the data in
Photograph by Bashford Dean. the following paragraphs.
A MATURE OVARIAN EGG
Such an egg is shown in Figure 1, plate I. In the original drawing, it measures
90 x 96 mm., and it was presumably drawn in natural size. It is of approximately the
same size as the eggs in round capsules shown in plate I. Its measurements are close to
those of eggs with gastrulae or very young embryos described by Nishikawa and by Dean
as found in the uteri.
This egg (Figure 1, plate I) is enclosed in the egg follicle and is covered by the thin
peripheral membranes of the ovary. These membranes are folded into ridges shown as
The Embryology of Chlamydoselachus 549
light streaks in the figure. Follicular blood vessels are shown as a dark network. This
rich vascular network is concerned with the nutrition, development and growth of the
huge egg. The circular area in the upper part of the figure is presumably a thin region of
the ovarian membranes where the follicle will rupture to allow the egg to escape into the
body cavity. It would seem that this egg is practically mature.
Among Dean’s records I find a photograph (Text-figure 12) of an ovarian egg. Study
of the detailed markings in drawing and photograph shows both to have been made from
the same egg. The drawing was probably made first, the photograph possibly after the
egg had been hardened and when a portion of the yolk had been torn away as shown in
the photograph. The text-figure is reproduced in the size of the original drawing so that
an accurate idea may be had of the natural size of this mature ovarian egg.
In this photograph the limits of the circular area shown in the upper part of Figure 1,
plate I, are more sharply defined. Similar areas are visible in five of the large but immature
eggs in the ovary shown in situ in Dean’s photograph referred to above. On ovarian eggs
Nos. 4 and 5, recorded in the list from Columbia University and mentioned ina preceding
paragraph, are found similar areas. Upon dissecting off the follicular membranes from the
circular area in one of these ovarian eggs, there was found a whitish region of correspond-
ing shape and size, which presumably represents the germinal area. This area is surround-
ed by a shallow depression—a circular groove. The remainder of the egg isa dark yellow
and appears to be composed entirely of yolk. I therefore conclude that the circular area,
represented in Figure 1, plate I, and in Text-figure 12, overlies the germinal area and is of
about the same size. It would be very desirable to study this egg but it cannot be found
among the specimens from Columbia University at my command.
When the ovarian follicles break, the ripe eggs in some way, as yet not clearly
understood, find their way into the funnel of an oviduct, and begin their descent into
this tubular organ in which fertilization, shell formation and gestation take place.
THE OVIDUCTS
As in other sharks, the oviducts are elongate paired organs joined at their anterior
ends where they communicate with the abdominal cavity through wide funnel-shaped
openings or sometimes through a single median aperture. Posteriorly each opens separate-
ly into the cloaca. When an egg gains entrance into an oviduct through the funnel, it is
fertilized by a spermatozoon, passes into and remains in the shell gland while the keratinoid
shell is being formed around it and then it descends into the uterine enlargement where
segmentation, gastrulation, and the formation and growth of the embryo take place.
There will now be considered some interesting features relating to these divisions of
the oviduct.
THE ABDOMINAL OPENINGS.
In Chlamydoselachus the abdominal openings of the oviducts are of particular interest
because of their variability. These variations will now be pointed out.
In Garman’s specimen (1885), each oviduct (Text-figure 8) has its own opening
widely separated from the other. Hawkes (1907, p. 475) does not state how many female
550 Bashford Dean Memorial Volume
specimens she examined, but she describes the funnels as follows: ““The oviducts have
large funnels, which open ventrad to the stomach. . . . The edges of the funnels are ir-
regular and spreading, and are united in the median ventral line to one another, thus
forming one large funnel. The anterior edges of the funnels become united to the anterior
wall of the body cavity, whilst the posterior edges of the united fimbriae hang free.”
Deinega’s one specimen had a single unpaired opening. So also in three of Smith’s
specimens (including one that is sexually immature), the oviducts communicate with the
body cavity through a single opening (Text figures 10, 11 and 14). Ina fourth fish (which
is mature), the abdominal opening has become transversely elongated until it functions as
two separate openings—one for each oviduct (Text-‘figure 15). Momose’s specimen
(1938) had a single oviducal funnel.
In Dean’s notebook is a good outline drawing, in pencil, evidently intended to form
the basis of a complete drawing. This shows a single large common abdominal opening of
both oviducts. In this respect, his specimen resembled those described by Hawkes (1907)
and by Smith (1937).
THE SHELL GLAND ~
The uterine egg of Chlamydoselachus is enclosed in a keratinoid shell. This is
secreted by a gland, the shell or nidamental gland, which is an enlargement of an anterior
portion of the oviduct. The glands of the two oviducts may be at the same level, as in
Smith’s immature specimen seen in Text-figure 10 and in Dean’s rough sketch showing the
oviducts and the two ovaries with large eggs.
In contrast, in Garman’s specimen (Text-figure 8), the left gland was anterior to the
right. So also was it in Smith’s three sexually mature fish as portrayed in Text-figures 11,
14 and 15. Deinega (1925) merely states that the shell gland of the right oviduct of his
specimen was placed somewhat further back than the left. This asymmetric position of
the shell glands (the left further forward) appears to be an adaptation to the slender form
of the body of Chlamydoselachus, and is probably correlated with the fact that the right
uterus is always functional and occupies much of the hinder abdominal cavity.
In Garman’s fish (1885) the shell glands were of about equal size (Text-figure 8), as
they are in Dean’s sketch showing them and the ovaries with large eggs. Concerning
this matter, Nishikawa says.*... the nidamental gland of the right side is better developed
than that of the opposite side”, but he does not say how many specimens he examined.
Smith graphically shows (Text-figures 11, 14 and 15) that in three sexually mature females
the right gland was noticeably better developed, and Deinega (1925) states this for his one
fish. Why the right gland is the better developed will be understood when the uterus has
been considered.
Garman (1885) figured and first described the internal structure of the nidamental
gland (Text-figure 13 herein). Here is his description.
The gland consists, in appearance, of two thick plates of laminated structure. The
plates are longer and thicker in the middle, and shorter and thinner at each side. The short
sides have been applied and united; this leaves an acute point descending from the thicker
The Embryology of Chlamydoselachus 551
portion on the inside of the tube. The insides of the walls are crossed by minute striae, be-
tween the laminae, which appear transverse, but in reality are spiral and ultimately—
following the outlines of the anterior or posterior borders—terminate, forward and back-
ward, in the longitudinal folds of the tube itself. The inner edges of the laminae are set with
minute pores. Near the middle of its length there is a deeper transverse groove. This is
crossed by the laminae without change in their directions on its account. The plates are not
distinct from each other through the whole of their length; branches frequently cross obliquely
from one to the other. The bottoms of the grooves between them have closely-set transverse
partitions. The walls of the gland are thicker anteriorly; they begin abruptly or even extend
a little in front of their points of attachment to the tube. The appearance is such as would
result from twisting the inside walls of the duct very closely for a short distance. In this we
have a hint as to the origin of the gland.
QA \
Text-figure 13
Interior of the shell gland of the frilled shark, Chlamydoselachus anguineus. Note the laminated structure.
Printed from the original woodcut after the drawing by Paulus Roetter for Garman, 1885, Fig. C, pl. XX.
This is not very clear nor does Garman’s figure (Text-figure 13 herein), devoid as it is
of explanatory lettering, help matters much. However, both must be reproduced here;
the text because it is the only full description ever published, and the figure because it
is the only one on record.
This gland has also been studied and described by Hawkes (1905) and it seems well to
quote her brief description. She gives no figure.
For the first 6 cm. the oviduct is a straight tube, the walls of which are lined with
numerous laminae. This region passes into the oviducal gland, the walls of which are much
thickened, except along two longitudinal lines which are approximately dorsal and ventral.
The length of the gland is 3 cm. Its interior is covered by fine laminae continuous with those
in the preceding and succeeding portions of the oviduct. The laminae run spirally, and are
very close together, instead of longitudinally and somewhat separated, as is the case throughout
the remainder of the oviduct. The transverse deeper groove in the oviducal gland mentioned
by Garman was found in the specimen examined. Passing from the oviducal glands, the
oviducts regain their original diameter, but the walls are smoother, the laminae being reduced
to slight striae.
552 Bashford Dean Memorial Volume
Unfortunately, after more than 30 years in preservative, the condition of the speci-
mens in the American Museum is such that the internal structure of the shell glands can-
not be studied advantageously.
THE UTERUS
In all viviparous sharks, the hinder part of the oviduct is enlarged into a more or less
capacious sac in which are received the fertilized ova when they pass downward from the
shell gland. Here the embryos undergo their development and here they are retained
until the shells are cast off and until the young are so far developed that they may be
passed out into the sea to fend for themselves. To fit the uteri for these purposes, they
are much modified in various sharks and rays, and marked differences arise in the function-
ing of the right and left organs. This asymmetrical functioning we shall now study in
Chlamydoselachus.
Ricut Uterus FuncTionar
Since the oviducal apparatus of a shark is bilateral, one might expect to find the two
oviducts equally developed in Chlamydoselachus. And so they are in sexually immature
females such as Smith’s 1398mm. fish (Text-figure 10). In a footnote to Nishikawa’s
article (1898), Goto says, “When no eggs are contained there is no perceptible difference
in size between the two oviducts.”” Such also is the condition shown in Momose’s
figure (1938) and much more clearly in the sketch sent me (Text-figure 9). This condition
is rather unexpected in this fish when one views the 80-mm. eggs contained in both
ovaries (Text-figure 9). That this condition is not always and necessarily true when eggs
are absent from the oviducts is seen in Smith’s drawing (my Text-figure 11) of the oviducts
of his 1550-mm. specimen. This fish was almost sexually mature but like Goto’s specimen
was nonbreeding. The right oviduct (Text-figure 11) was noticeably larger than the left,
and the ovaries contained growing eggs up to 17 mm. in diameter. Presumably the right
uterus only in this fish was destined to be functional.
Our earliest information concerning the inequality of development of right and left
oviducts in the frilled shark comes from Samuel Garman (1885), the man who first dissected
Chlamydoselachus. In his specimen, which had been partially eviscerated, the anterior
portions of the oviducts (about 12 in. long) remained as shown in his drawing (Text-figure
8 herein). But of the hinder end he was fortunately able to say—“A piece left at the
cloaca showed one of the ducts greatly distended, possibly with young that had hatched
within it [or which had been removed before the specimen came to him]. Only one of
these tubes had been in use”.
Next comes Collett (1897) who states that in his 1910-mm. fish each oviduct was
900 mm. long, and that “Towards their upper [lower ?] ends each expands to a uterus-like
sack of which the right is somewhat larger than the left; both contained immature eggs’.
As noted above in the section on the ovaries, Collett or his translator got his identification
of organs mixed, and here as there I have supplied the correction in brackets. His state-
ment that both oviducts (the right being better developed) contained eggs, even if im-
mature, is significant. It will be referred to later.
The Embryology of Chlamydoselachus 553
In 1898, Nishikawa gave us our first definite data on the inequality in structure and
function of the oviducts. He states that the left one is always rudimentary but that
‘The right oviduct is very much distended and contains from 3 to 12 eggs, these numbers
being the limits observed in 7 specimens”.
Hawkes (1907) notes that the right oviduct in her specimens was much larger than
the left. So Smith found and graphically shows for three fish in Text-figures 11, 14 and 15
herein. The uteri of Hawkes’s specimens contained no embryos; nor did Smith’s. Since
Smith’s specimens were brought from Japan by Dean, it is probable that, when the two
gravid fish were caught, the uteri (Text-figures 14 and 15) were opened to get the eggs and
embryos for him.
Deinega (1925) was evidently under the impression that Chlamydoselachus, like
most other sharks, should carry eggs and embryos in both uteri. He states that in his
specimen “‘the left oviduct, in its exterior form, produces the impression of being under-
developed or of being in a temporarily non-functioning condition”. However, the right
oviduct, a short distance behind its large shell gland, “suddenly expands into a rather
capacious sac”. It contained no eggs.
Dean’s notes afford both negative and positive evidence of the differential function-
ing of the oviducts. Thus of a 1565-mm. fish he says, “left ovid. greatly reduced, eggs
fr. r.”; of a 1575-mm. female he notes “left ovid. greatly reduced, no dilat. uterus”;
another 1565-mm. fish had “‘l. ovid. small, small uterus’. On the other hand Dean
records the taking of various eggs and embryos from the right oviducts of specimens of
Chlamydoselachus captured in the Sagami Sea. From one fish he got two eggs and from
another three. Then he notes ‘‘8 in female”—oviduct not recorded but presumably the
tight. As seen above, and as will be noted later, had it been the left he would pretty
surely have so stated. In the records of his Japanese collector are listed three eggs from
right oviduct of one fish, five from another, and seven from the right oviduct of each of
two other females. These last eggs were all in early stages and had egg shells.
DisTENTION OF Gravip Ricut Urerus.—Unfortunately there are little data available
as to the size attained by the right uterus as gestation goes forward to birth. However,
there are two ways of studying the problem: one by bringing together the few scattered
measurements of the organ, the second by setting forth the number of eggs and embryos
(with their measurements) found in the uterus. These compilations will now be made.
Measurements of Gravid Right Uterus.—Hawkes (1907) states that the oviducts
begin to enlarge when they reach the level of the anterior end of the colon. On the left
the diameter is increased gradually and only about four-fold, but “‘on the right, the en-
largement is sudden and very apparent, the diameter increasing 14 to 15 times”. She
nowhere speaks of finding embryos in the uterus.
Deinega’s description (1925) of the reproductive system is very brief. But the two
things that the reader gets from it are that the left oviduct ““produces the impression of an
underdeveloped oviduct or a temporarily non-functioning one”. While the right one in its
posterior part “suddenly expands in the form of a rather capacious sac about 130 mm. in
554 Bashford Dean Memorial Volume
diameter”. This very great expansion is clear in his figure which, however, is so poorly
printed on soft paper that it cannot be reproduced here.
Smith dissected and figured the reproductive organs of two sexually mature frilled
sharks measuring 1350 and 1485 mm. respectively. He does not give measurements of the
oviducts but Text-figures 14 and 15 give the relative sizes of the oviducts and other organs.
Urogenital system of the female Chlamydo-
selachus, ventral views, one-fifth natural size.
The shell glands and the adjoining portions of
the oviducts are displaced laterally.
Text-figure 14. Urogenital organs of a speci-
men 1350 mm. long. The right uterus and
ovary are incomplete.
ab.p., tight abdominal pore (the left is closed superfici-
ally); c.t., collecting tubule; m., mesonephros; mes.d.,
mesonephric duct; mso., mesovarium; ovd., oviduct; ovy.
ovary; 7. cl., rectal portion of the cloaca; s.g., shell gland;
ur.p., urethral pores; ut., uterus; v.l., ventral ligament
of the oviduct.
Drawn from specimen No. I in the American Museum
of Natural History.
After Smith, 1937, p. 433.
Text-figure 15. Urogenital organs of a speci-
men 1485 mm. long. A segment has been
excised from the right uterus, and the right
ovary is incomplete. The excretory ducts are
not shown.
ab. p., abdominal pore; m., mesonephros; ovd., oviduct;
ovy., Ovary; 7., rectum; s.g., shell gland; ur.p., urethral
pores; ut., uterus; v.I., ventral ligament of the oviduct.
Drawn from specimen No. II in the American Museum
VN of Natural History.
After Smith, 1937, p. 433.
unp.
Text-figure 14. Text-figure 15.
These fish had evidently been gravid and the enlarged right uterus of each had been opened
and the eggs removed. These adults (and probably the eggs also) came to Dean—presum-
ably at Misaki, or were later sent to him in America.
In Dean’s notebook is a rough sketch of the reproductive apparatus of his huge 1960-
mm. female. This shows the two ovaries with many eggs (elsewhere referred to) and two
empty uteri—the right twice as large as left. (Here recall Smith’s drawing, my Text-
The Embryology of Chlamydoselachus 555
figure 11, showing similar organs). On this page, above Dean’s sketch, is the statement
“Ovid. [uterus?| of r. [side] dilated [through a length of] 340 mm.”. Two pages away is
another and more elaborate sketch of a non-gravid right oviduct (previously referred to)
in which the uterus is labelled 25 mm. wide and 280 mm. long.
None of these specimens (except Nishikawa’s) had ova in their uteri, and none of
these uteri save those figured by Deinega and by Smith give us any clear idea of the size
and the degree of distention attained before the young are born. However, some under-
standing of the degree of this dilation may be had by considering the number of eggs and
embryos (with their measurements) that have been found in some gravid uteri. Earlier in
this article some of these data have been used for other purposes but for completeness they
will have to be repeated here.
Number of Eggs and Embryos in Gravid Right Uterus.—From two men only do we
get firsthand data as to uterine embryos and their yolk sacs. Nishikawa introduces us
to the subject briefly. But from Dean’s notebook and from specimens brought back from
Japan or sent thence to him, we get a good idea of the great size of eggs and embryos and
of the uterine distention to which they give rise.
Nishikawa (1898) says “The right oviduct [600 mm. in total length] is very much
distended . . when as many as 12 eggs [his upper limit] each 110-120 mm. long are con-
tained in it”. Some of his eggs had embryos—the largest only 60 mm. long. He also
speaks of having other eggs 65 to’75 mm. in shortest diameter and from 102 to 124 mm. in
longest measurement. He figures in natural size an egg (Text-figure 4 herein) 67 x 100 mm.
in an egg shell measuring 137 mm. including the processes.
Of large uterine embryos, Dean lists 14 specimens ranging from 165 to 390 mm.
(6.6 to 15.35 in.). Of these only two have measurements of the yolk sacs set down.
However, Dean brought from Japan and deposited in the zoological museum of Colum-
bia University three embryos with yolk sacs, and in the American Museum six embryos
with yolk sacs. From the Museum of Comparative Zoology, there has been loaned a large
embryo on its yolk sac. This was presented by Dr. Dean in 1912. The measurements of
these embryos with yolk sacs give one a full conception of the distention they would
produce. They will be considered later, but it may be well first merely to list the embryos
without yolks.
Dean’s notebook records 12 such fishlets. To these I have added a specimen (190
mm.), in the collection here, from which the yolk has been removed. The measurements
of these little fishes are from snout to tail tip. These 13 range from 165 to 352 mm.
(6.5 to 13.8 in.) as follows—165, 175 (2 specimens), 185 (2), 190, 195, 205, 210, 240, 250,
317, 352 mm.
To get a better idea of the distention of the gravid right uterus one must consult
table I wherein are listed embryos ranging from 170 to 390 mm. (6.7 to 15.35 in.). These
sit on yolk sacs whose diameters (measured in the lines of length and depth of the fish)
vary from 67 x 55 mm. (fish, 327 mm.), to 111 x 100 (fish, 331 mm.), to 73 x 51 (fish, 374
mm.). With from 8 to 12 of these contained in the slender body of this snake-like (anguin-
eus) shark, one can judge the enormous enlargement of uterus and abdomen.
556 Bashford Dean Memorial Volume
TABLE I
SIZES IN MILLIMETERS OF UTERINE EMBRYOS AND EGGS
|
| No. | Embryo Yolk Sac Where
1 | 170 | 72x68 | Columbia University
2 175 | 92x90 | Figure 11, plate I
3 180 77x75 | Columbia University
4 210 75x57 Am. Mus. of Nat. Hist.
5 210 85x66 Mus. of Comp. Zool.
6 245 74x60 Am. Mus. of Nat. Hist. |
7 305 83x57 baie ne seacct IPs
8 320 76x64 | 4 meee
9 327 67x55 | Columbia University
10 331 111x100 | Dean’s Notebook |
11 374 73x51 | Am. Mus. of Nat. Hist.
| 12 390 100x70 | Figure 49, plate V.
Just here it should be recorded that in Dean’s notebook on the page of his list of
specimens to be drawn is this entry. “Bt. in Tokyo June 20: 317; 331, yolk sac 111 x 100;
352; 390, yolk sac 100 x 70; 4 embs. large taken about May 1, 1905. 8infemale”. I judge
that the “4 embs. large” refer to the four for which he gives sizes, that they were taken
from the female captured May 1, that they were preserved, and that he purchased them
June 20 in Tokyo. This seems pretty certain. Possibly they were 4 of the “8 in female”
as noted. Judging by their close gradation in size, I conjecture that they came from one
uterus. If so, one can judge the tremendous distention of this. But what if one uterus
contained “8” such embryos and eggs! It seems almost unthinkable, yet Nishikawa
(1898) says “The right oviduct is very much distended and contains from 8-12 eggs... .
The limits observed in seven specimens.”
Two of the specimens recorded in the table were drawn for Dean and are reproduced
in the plates. In Figure 11, plate I, the embryo measured 175 mm. and the yolk 92 x90 mm.
Still more striking is the colored Figure 49, plate V of a fish 390 mm. (15.35 in.) long on
a yolk sac which measured 100 x 70mm. Let the reader imagine (if he can) 8 to 12 embryos
and yolk sacs of this size in the uterus of even a 1960-mm. female (the largest Chlamydo-
selachus on record). The egg and embryo of the colored figure are in our collection here,
and the fish in its jar of alcohol looks even larger than it does when portrayed in its
natural colors.
As one studies this table, three things attract attention. The first is that there are
several discrepancies in the sizes of the yolk sacs in proportion to the sizes of the little
fish found thereon. Surely some of the discrepancies date back to the varying sizes of
eggs in the ovary. There must be more variability in the size of mature eggs in the
oviduct than has heretofore been thought. The next idea is that the period of gestation
must be very long to give time for the resorption of these great yolks, and then that the
young fish when ready for extrusion must be from 20 to 25 in. long. The matter of
the long period of gestation (surely at least 2 years) has been treated earlier.
The Embryology of Chlamydoselachus 557
The third matter is also based on the great disparity between the slight diminution of
the yolk sac and the considerable growth of the embryo. It comes to me in this form—
Does the embryo of this viviparous or ovoviviparous shark receive any nutriment from
the uterine wall of the mother? The shallow water littoral tropical nurse shark, Gingly-
mostoma cirratum, is also ovoviviparous. It carries in its uteri huge (c. 145 mm. long)
blunt-ended, thick-shelled eggs (Text-figure 16) entirely comparable to those of Chlamydo-
selachus. I have had the good fortune to make extensive studies on Ginglymostoma, the
nurse shark, and from these I hope further on to throw light on this question.
All these data (save those from Deinega’s article) were known to Smith when his mo-
nograph on the anatomy of Chlamydoselachus was published in 1937. But in the matter of
the reputed unilaterality of the functioning of the oviducal apparatus of Chlamydoselachus,
he showed sound judgment in his concluding remarks on the reproductive organs of
the female of this shark. Here is his matured statement published before I had made
my minute study of Dean’s notes presently to be referred to. Smith (1937, p. 449)
wrote as follows:
There is not a single known instance of complete development of the reproductive organs
on the left side. Yet it must be borne in mind that the number of specimens that have been de-
scribed is still very small. The organs on the left side are developed to such a degree that
they can scarcely be called rudimentary. In view of the great variability found in many
other organs of Chlamydoselachus, one should not be surprised if the examination of ad-
ditional material should reveal cases in which the genital organs of the left side, or of both
sides, are functional.
In the light of the data given above as to the functioning of the right oviduct only in
Chlamydoselachus, there are now to be presented certain data showing that the left ovi-
duct also is sometimes functional in this shark. In these data will be found the verifi-
cation of Smith’s prognosis.
Tue Lert Urerus Sometimes FUNCTIONAL
It has already been seen that in the adult, while the right ovary is the predominant
one, the left ovary does sometimes contain large eggs; i.e., is functional. Evidence that
the left uterus is occasionally functional will now be presented. This is a matter of ex-
ceptional interest.
The earliest intimation, that the left oviduct may contain eggs, comes from Collett
(1897). In his short and not always clear description of the oviducts of a 1910-mm.
specimen, he says that “each expands to a uterus-like sack, of which the right is somewhat
larger than the left; both contained immature eggs”. There is no doubt that he was
referring to the oviducts, but what he meant by “immature eggs” is very obscure. I can
only conjecture them to have been wind eggs like that figured by Dean (Figure 51, plate
V). In many years’ dissections of viviparous sharks and rays, I do not recall ever having
found in a uterus an “immature” egg, meaning an undeveloped or unripe or shell-less egg,
but I have in the nurse shark found what my notes record as “infertile eggs”. I do not
recall that I opened one to get at its contents. I did not then know of the term “wind
558 Bashford Dean Memorial Volume
eggs’, but that is what these eggs were. I measured a number of these capsules from
Ginglymostoma and found them always smaller than normal (fertile) eggs such as that
shown in Text-figure 16.
The only other evidence of bilateral functioning of the oviducts-in Chlamydo-
selachus is found in Dean’s notebook. In one place he says of a 1620-mm. specimen “both
ovid. same size’, but he does not say that both were functioning. They may have been
found in a sexually immature fish such as Smith had (Text-figure 10). However, from a
1392-mm. female taken about October 1, 1905, Dean records “*3 oblong eggs, 135 mm. and
larger in r. ovd.”’ and a “‘small wind egg in 1.”. He states that two oblong eggs and the
wind egg were drawn. The two oblong eggs I identify with the drawings shown in
Figures 2 and 3, plate I; and the wind egg as that portrayed in color in Figure 51, plate V.
From another female taken May 25, 1906, Dean records eggs “‘l. ovd. 3, 2 in r.” but
unfortunately he gives no description of these eggs.
It is very interesting and possibly significant that, so far as we have data, when eggs
are found in both oviducts of Chlamydoselachus, there is something wrong with them.
According to Collett both sets of eggs from his fish were “immature’’—whatever that
may mean. In Dean’s first case, the egg from the left uterus was abnormal—an empty
dwarf shell—while the eggs from the right side were at least unusual if not abnormal. All
three were “oblong”—two of them in varying degrees, (Figure 2 and 3, plate I). One
(Figure 2) is oblong but symmetrical, the other (Figure 3) is not only oblong but unsym-
metrical, and is possessed of a most unusual process. Of the eggs from the two oviducts
of his specimen taken May 25, 1906, Dean unfortunately gives neither figures nor
descriptions.
As bearing on this matter, it may be noted here that the nurse shark has the right
ovary only fertile but both uteri functional. Infertile wind eggs, always smaller than
fertile ones (size about 105 mm. long by 120 in circumference) are found in both uteri of
this shark, but are apparently more abundant in the left.
One wishes much for definite data here about Chlamydoselachus. What were
Collett’s “immature eggs?” What kind of eggs were those noted by Dean in the “l. ovid.
3°? Were they defective? The predominance of the right oviduct is of course correlated
with the narrow abdomen of this “‘snake-like’”’ shark—there is not room in the crowded
abdominal cavity for two gravid uteri. Yet Dean states that he found such in two speci-
mens. Here isa problem for someone in Japan to solve.
These data from Collett and from Dean show us that the commonly accepted dictum,
that the right oviduct only in Chlamydoselachus is functional, is not always true, even
though all other investigators have so found or thought. Since Dean’s notes show that
the “I. ovid.” is sometimes functional, they have been quoted carefully and in full. Into
Dean’s hands there undoubtedly came more female specimens (26 in number) than have
been had by all other students of Chlamydoselachus taken together. This of course made
possible his discovery of the functioning of the left oviduct in his two specimens. Un-
doubtedly this functioning is very unusual and apparently it is not wholly normal.
The Embryology of Chlamydoselachus 559
But in any case, we are sure that, in some few instances, Chlamydoselachus does have
both oviducts functional.
Here then is confirmation of Smith’s statement (1937)—“‘In view of the great varia-
bility found in many other organs of Chlamydoselachus, one should not be surprised if
examination of additional material [Dean’s 26 female specimens] should reveal cases in
which the genital organs of the left side, or both sides, are functional”. And all through
his work, Smith points out generalized or primitive structures in Chlamydoselachus in
consonance with the lowly position assigned it in the scale of shark life. Then again he
finds highly specialized structures.
Chlamydoselachus is in process of becoming viviparous by getting rid of its primitive
keratinoid egg shell—it has almost gotten rid of the hold-fast processes. Then further to
make possible this viviparity in a small and narrow body cavity, it has almost achieved
unilaterality in the functioning of its reproductive organs.
For comparison, evidence will later be presented to demonstrate that in certain
higher viviparous sharks and in certain rays (highly specialized elasmobranchs) the
unilaterality found imperfectly expressed in Chlamydoselachus has come to full fruition.
There is now to be considered certain indefinite evidence referred to above—the
question whether the embryos of Chlamydoselachus are nourished by secretions from
the wall of the maternal uterus.
Do Emsryos Receive NutriMeNT From THE UTERINE WALL?
On this point Hawkes (1907) writes of the enlarged (uterine) portion of the right
oviduct as follows:
This region in addition to being enlarged has folded walls, in which occur one large
and several small areas of dilated blood vessels. The largest blood plexus occupies about
one-third of the right side of the oviduct. In connection with each plexus, on its dorsal side
the oviducal wall is thickened over an area which equals the plexus in length and breadth.
The enlarged vessels apparently supplied these thickened areas. The condition of the
oviduct thus described suggests that this portion of the oviduct acts as a functional uterus.
Smith had hoped by study of our specimens to throw more light upon the internal
structure of the uterus as described by Hawkes. But he had little success. He notes,
however, (1937, p. 447) that—‘‘In its enlarged state, on the right sides of my adult
specimens, the so-called uterus has thin walls, a velvety inner surface and a fairly rich
blood supply. The mucous membrane is not sufficiently well preserved to permit a study
of the finer structure”.
To anyone with a firsthand knowledge of the structure and functioning of the uterine
wall of viviparous sharks and rays, these findings are very significant. From a mere
glance at Figure 49, plate V, it is apparent that there will never be a yolk-sac placenta
connection between embryo and mother in Chlamydoselachus. If the uterus nourishes
the embryo, this must be accomplished in some other way. In the hope of getting some
560 Bashford Dean Memorial Volume
light on this obscure problem, let us now examine the uterus of that ovoviviparous shark
whose reproduction most nearly parallels that of Chlamydoselachus.
The tropical shallow-water nurse shark, Ginglymostoma cirratum, carries in each
greatly dilated uterus as many as 21 huge thick-shelled eggs like that shown in natural
size in Text-figure 16. The inner wall of each uterus is made up of circumferential bands
of hems or plaits overlapping like the shingles on a roof. The plaits are 5 or 6 mm. wide
and are highly vascularized—“as red as a piece of fresh-cut beefsteak” my notes read.
Textfigure 16
The egg case (140 mm. long), egg, and embryo of the ovoviviparous nurse shark, Ginglymostoma
cirratum—in natural size. Note the left, older, more finished looking end of the capsule and the
larger, blunter, younger right end. The yolk blastopore is seen just to the right of the tail of
the embryo.
Photograph by Alfred Goldsborough Mayor.
We have no statement of the collectors that embryos and their yolks are found in the
uteri of Chlamydoselachus free of their shells, but it is evident that an embryo even as
relatively young as that shown in Figure 11, plate I, or as old a one as that shown in
color in Figure 49, plate V, has thrown off its heavy egg capsule. These large broken
capsules could not be carried in the uterus without hurt to the delicate embryos. They
must be thrown out into the sea. Similar reasoning must be applied to similar conditions
in the nurse shark and its embryos enclosed in a larger and thicker egg shell.
The boatmen at the laboratory of the Carnegie Institution of Washington at Tortu-
gas, Florida, where my studies were made, were all Florida and Bahama men, well ac-
quainted with the nurse shark. They all told me that when the young are pretty well
developed, they break out of the shells, and these latter are cast out while the embryos are
The Embryology of Chlamydoselachus 561
retained in the uteri during further development. I was told by the director, Dr. A. G.
Mayor, that this was his understanding, but after these years I cannot recall if this was
his personal observation. I was never fortunate in procuring large embryos nor small
free-swimming young. Development is slow and the advent of the hurricane season led
to the closing of the laboratory late in July of each year before the slow-developing eggs
had gone far enough for the embryos to break out of their shells.
The young and growing fishes in the uteri of these two viviparous sharks must have
oxygen. If sea water could penetrate the cloaca and into the uteri, it might provide this
need. The nurse shark has a wide cloaca and the oviducal opening into it will sometimes
admit “three or four fingers bunched into one mass”, as my notes read in one case, and in
them it is also recorded that a female Ginglymostoma hung up by the tail had the common
oviducal opening measuring 1.5 in. in diameter. The opening must be this large to admit
the outward passage of the large empty egg shells even if crumpled. Furthermore, I have
opened a uterine egg of the nurse shark and on tasting the perivitelline fluid have found
this salty. The embryo was very young.
I unwittingly performed another experiment which demonstrated that the egg
capsule of Ginglymostoma is permeable to sea water. I took an egg capsule with its
lively embryo out of the uterus of a just-killed female, cut a window in the capsule over
the embryo, cleared out all the perivitelline fluid that I could and replaced it with mo-
lecular magnesium sulfate in order to anesthetize the embryo. The egg was then unthink-
ingly placed in a dish of sea water which did not cover the window. Twenty-two hours
later the little shark was about as lively as ever. The sea water had penetrated the egg
shell by osmosis and had so diluted the anesthetic solution that the embryo still lived.
There seems to be little doubt that the embryos of Ginglymostoma may get oxygen
from the sea water which may come into the uterus through the dilated cloaca and the
large oviducal openings. No experiments such as those above have been performed on
Chlamydoselachus, but Dr. Smith tells me that the cloaca is open in his preserved speci-
mens and that the right oviducal opening even when hardened in formalin will sometimes
admit a man’s thumb. So one may conjecture that sea water invades the uterine cavity of
Chlamydoselachus and bathes the eggs. Thus the embryo could get oxygen from this
water.
On the whole it seems quite probable that the young of both sharks may receive some
oxygen by diffusion from the uterine wall into the fluids surrounding the embryo. Fur-
thermore, from my knowledge of uterine gestation in other sharks and in various rays, |
am strongly of the opinion that the uterine wall in both Chlamydoselachus and Ginglymos-
toma secretes liquid food materials to nourish the young after they are freed from the egg
capsules. As shown in Figure 34, plate III, and Figure 43, plate IV, the embryos of
Chlamydoselachus have short external gills, gills far shorter than I have found in the
young of some viviparous sharks and particularly of various rays. Presumably the young
of Ginglymostoma also have such gills. The long external gills of embryos of rays and of
other sharks, when bathed in the uterine fluid, may take in not only oxygen but mineral
62 Bashford Dean Memorial Volume
OW
salts and possibly other food substances as well. The rich plexus of vitelline capillaries
will also be bathed in the fluid of the uterine cavity and they may absorb some food and
oxygen from it. If this takes place in Chlamydoselachus, it must go on for a long time,
until and even after the yolk, shown in the colored Figure 49, plate V, is resorbed, and
this yolk must be used up before the fish is born, else the free oceanic life of this little
shark would be very brief.
THE CLOACAL OPENINGS
As has been shown, the oviducts at their anterior ends have openings into the ab-
domen to receive the eggs set free from the ovaries. So, posteriorly the oviducts have
openings into the cloaca through which the embryos, having used up their yolk masses in
development, pass out to take up their free life in the sea. The lower end of the uterus
progressively diminishes in size until, as a tube considerably reduced in cross-section, it
opens out on the dorsal side of the cloaca. But even here, as everywhere else in this
primitive shark, are found some surprising and interesting variations.
Ricut Croacat Ovipucat Orentne PRrepominaNt
Since the right oviduct is predominant, since its uterine portion carries the develop-
ing young, and since these must pass out through its opening into the cloaca, one would
expect to find that the right opening is larger and is possibly somewhat centrally placed.
Hawkes (1907) first and very briefly refers to the relative sizes of the oviducal
openings into the cloaca thus: “The opening of the right enlarged oviduct . . . has
acquired a median position, the left oviducal opening . . . lying cephalad to it”. Only
this, but she gives a diagrammatic figure to make these relative positions clear —Text-
figure 17 herein. Deinega (1925) confirms Hawkes and writes at length. Thus he says
“The right oviduct opens out by a large orifice in the middle of the cloaca”—as is shown
in Hawkes’s figure. Of the opening of the left oviduct he writes more fully “The left
oviduct opens in the dorsal wall of the cloaca, rather far in front, so that it makes an im-
pression as though it opens into the posterior section of the right oviduct; this orifice
appears in the form of a cross fissure”.
Text-figure 17
Diagrammatic figure of the cloaca of
a female Chlamydoselachus.
A.P. closed abdominal pore; L.Ov., leit
oviducal opening; R., rectum; R.G., opening
of rectal gland into rectum; R.Ov., night
oviducal opening; U.S., urinary sinus (the
other sinus is omitted); U.S. 1, openings of
urinary sinuses into cloaca.
After Hawkes, 1907, p. 476.
The Embryology of Chlamydoselachus 563
Textfigure 18
Longitudinal section through cloaca and right oviduct of Chlamydoselachus,
three-fourths natural size. The dorsal side is uppermost.
ab-p, abdominal pore; cl, cloaca; int, intestine; ov, oviduct; p, caecal pouch or rectal gland; ua,
urethral aperture.
After Garman, 1885, Fig. 2, pl. XIX.
The relative positions of the two openings as stated by Deinega make somewhat
clearer these openings as portrayed in Garman’s drawing (Text-figure 18) of the cloaca of
his specimen. If one holds the page in the vertical plane in the line of vision with the
dorsal side of the figure uppermost and the cloacal end toward the observer, the relations
will become clearer. The right lateral wall of the right oviduct (ov in the light area) has
been cut away near the point of junction of the left oviduct (ov in center in dark area).
The figure shows a common tube leading into the cloaca. From this, it is seen that the
left oviducal opening is situated in the wall of the right aperture.
Smith found the two openings in all his specimens, but, excepting in the youngest,
the right opening was predominant. This was markedly true in his two sexually mature
females as shown in Text-figures 14 and 15. In the cloaca in each figure the large shaded
area on the (fish’s) right side is the opening of the right oviduct, the smaller shaded area
on the left the opening of the left tube. Note how very predominant the right opening
is in Text-figure 15. Here is Smith’s statement on this condition in the fully mature
specimen referred to: “.. . almost the entire urogenital sinus seems built around the very
large opening of the right uterus indicated by line-shading in the figure [No. 15 herein].
In the hardened condition of the material, this opening is still large enough to admit
a thumb. The opening of the left uterus is much smaller’.
Here again is further proof of the unilaterality of functioning of the right oviduct of
the frilled shark. Shell gland, uterine enlargement, posterior opening into cloaca, each
overshadows its fellow on the left.
564 Bashford Dean Memorial Volume
FEMALE REPRODUCTIVE ORGANS OF CERTAIN HIGHER SHARKS
AND VARIOUS RAYS
For the frilled shark, Chlamydoselachus, it has been shown that unilateral functioning
of the reproductive organs is the general rule, that the right ovary and oviduct are uni-
formly fertile, but that rarely are both organs on the left side also functional. I have made
some studies on this subject of unilateral functioning of reproductive organs based on
dissections of sharks and rays at the U. S. Fisheries Laboratory at Beaufort, N. C., and in
the reports on these (Gudger, 1912, 1913) I have given references to a number of articles
bearing on this subject. To all these the interested reader is referred.
The records of my studies on the reproductive organs of sharks and rays dissected at
Key West and at Dry Tortugas, Florida, while a guest-investigator at the marine labor-
atory of the Carnegie Institution of Washington, have never been published. Since some
of these notes bear directly on the subject in hand, and particularly since one of the sharks
(Ginglymostoma cirratum) in its eggs and reproductive apparatus shows certain marked
likenesses to these structures in Chlamydoselachus, it seems well to quote from these
notes here.
OVARIES AND OVIDUCTS OF SOME FLORIDA SHARKS
Since the sharks examined in southern Florida show the least departure from their
early ancestors in the bilaterality of their reproductive organs, they will be studied first.
The first departure from bilaterality like that noted in Chlamydoselachus has to do with
the ovary.
The Nurse Shark, Ginglymostoma cirratum.—In eight dissected female specimens of
this large, flat-bodied, sluggish, shallow-water shark with a large abdomen, both oviducts
were always functional, but in each fish the right ovary only was functional. The fish were
adults about 8 ft. in length, “over all”. One had in the right ovary “30 eggs the size of
small oranges (equatorial diameter=60-65 mm.)”. Another had 33 ripe eggs in the right
ovary. Still another had “right ovary enormously enlarged with 40 eggs size of billiard
balls, some about 6 in. in circumference. These would have filled a peck measure or an
ordinary water bucket”. Three had “right ovary full of gaping pits from which ripe eggs
had been erupted”. Nearly all these enlarged right organs were median in position, while
of the left ovary my notes say “insignificant in size”, “hardly recognizable”, “had to be
hunted for”. Not one left ovary had any eggs. It is to be regretted that none of these
huge right ovaries was measured.
Various Other Florida Sharks——The large, active, voracious tiger shark, Galeocerdo
tigrinus, has the oviducts bilateral and functional. In four fish the left ovary was generally
small and always non-functional, the right large, and functional with eggs in the anterior
part. I have notes for three species of the requin shark, Carcharhinus. In four specimens
of C. obscurus with bilateral functional oviducts, the left ovary was “small”, “very small’,
“reduced”; while the right was always large and functional. In one 8-ft. fish, it was 2 ft.
10 in. long with 12 eggs, .5 to 1 in. in diameter. In one specimen of C. falciformis, my
The Embryology of Chlamydoselachus 565
notes read “‘l. ovar. very small, r. nearly twice as large”. A solitary C. platyodon had
the left ovary small and the right large with eggs in the anterior part. Both these sharks
had both oviducts well developed and functional.
Of the genus Hypoprion, I dissected two species—H. brevirostris and H. signatus.
In each, the oviducts were bilateral and functional, but the left ovary was small and with-
out eggs; the right ovary was large and functional with eggs in the anterior end. The
same condition of oviducts and ovaries was also found in Scoliodon terranovae.
From these data on some of the tropical sharks of the eastern Gulf of Mexico, it is
plain that they are on the way toward unilateral functioning of the reproductive organs.
They have not gone so far in this matter as has Chlamydoselachus, since both oviducts
are functional while only one ovary (the right) produces eggs. No reason for this can
now be given, since they are sizable sharks with large abdominal cavities. This is especial-
ly true of the flat-bodied Ginglymostoma, in whose roomy abdomen are contained large
uteri which when gravid much resemble in size and shape a pair of old-fashioned saddle-
bags. This size and form make it possible for each to contain, or are conditioned upon its
containing, 20-21 eggs c. 140 mm. long x 185 in circumference. From these sharks with
partial unilaterality of genital organs, we now pass to the rays in some of which complete
unilaterality has been attained.
OVARIES AND OVIDUCTS OF VARIOUS RAYS
The rays are elasmobranchs flattened in the dorsoventral or vertical plane to fit them
for bottom-living. They comprise the most specialized group of the Elasmobranchii.
They are referred to here because there are found in these viviparous fishes the same vari-
ations in the reproductive organs that are found in Chlamydoselachus, the reputedly
lowest form of the strap-gilled fishes. There is an extensive literature on this subject
but I shall confine myself to my own researches.
Pteroplatea maclura.—The butterfly ray is abundant at Beaufort, N. C. In 1912
(Gudger, 1913) I dissected four female specimens. The reproductive organs of both sides
were functional, but in every fish the left ovary was better developed than the right
(in fish No. II, 25 per cent larger). Furthermore, in each case the left uterus was better
developed and contained more eggs. Fish No. I had three eggs in the left uterus and an
empty shell (wind egg) in the right; No. II had one egg (but with two yolks) in 1. and
an imperfect egg in r.; No. III had two eggs in 1. (one with a malformed shell) and one in
r.; No. IV had both uteri gravid but left twice as large as right. Unfortunately these
two uteri were not dissected.
It is significant that in this ray the reproductive organs of the left side are better
developed and more functional than those of the right. This is just the reverse of con-
ditions in Chlamydoselachus. Another notable point is that imperfect eggs are found in
both uteri of the ray. Parenthetically it may be noted that this same condition seems to
prevail in the nurse shark. From all these data, I draw the conclusion that Pteroplatea
maclura is in an intermediate stage between those rays having perfect bilaterality of the
566 Bashford Dean Memorial Volume
reproductive organs and those having only one side functional as in Dasyatis say now to be
briefly considered.
Dasyatis say.—The common stingray or “‘stingaree” also abounds at Beaufort, and in
1912 I reported the results of my dissections over a number of years. Sixteen non-breeding
females (uteri showing no signs of having eggs in them) ranging from 13 to 35 in. in width
had the left ovary from two to three times the size of the right. Thirteen breeding females
(13 to 35 in. wide) had the left ovary functional (with eggs 12-18 mm. in diameter) and
the left uterus greatly dilated—some with embryos, and some awaiting the coming of eggs.
In the course of several summers’ work, no right ovary was found with any eggs in it
and no right uterus was ever functional. These facts were paralleled by my studies of
another species of the same genus.
Dasyatis hastata.—This is the common stingray of southern Florida. At Key West
and at Tortugas, I dissected 10 specimens. Five were adults ranging from 3 to 4.5 ft.
wide. In these, the left uterus only was enlarged and functional (some with embryos).
In all, the right ovary was “insignificant” but the left was large and in many cases had
large eggs init. [also dissected five half-grown to adult specimens from 13 to 26 in. wide.
Even in these, the left uterus was large and seemingly ready to receive eggs, the right
reduced and indistinct. In all five the right ovary was small and non-functional. The
left was always larger (in the 26-in. ray ten times larger) and filled with growing eggs.
Here is described a progressive gradation from partial to complete unilaterality in the
functioning of the reproductive organs of elasmobranchs. In the butterfly ray, Pteroplatea
maclura, both ovaries and both uteri are functional, but in all dissections the left organs
were invariably better developed—.e., the right ones are beginning to degenerate. The
sharks described (Chlamydoselachus excepted) all have bilaterally functioning oviducts,
but unilaterality in the ovaries in that the right ones only are functional. Finally in the
stingrays, Dasyatis say and hastata, complete unilaterality is found—left ovaries and left
oviducts only are functional. Here then are those specializations in the functioning of the
reproductive organs which are adumbrated in Chlamydoselachus, the lowest ranking
shark and lowest elasmobranch. In the rays as in the frilled shark, there is found the
same correlation of unilateral genital organs with a restricted body cavity. In Chlamydo-
selachus, the body cavity is narrow but is somewhat long to contain the closely-packed
embryos; in the rays the cavity is both short and narrow and in the single uterus the
few embryos are rolled up scroll-fashion.
From other notes made from my dissections and from a rather extensive but widely
scattered literature, other similar unilateral functionings of ovaries and oviducts in other
elasmobranchs might be given if it seemed necessary to go into the matter further.
THE ENCAPSULED EGG OF CHLAMYDOSELACHUS
The encapsuled egg of Chlamydoselachus, as it emerges from the shell gland and
passes into the uterus, consists of a large yolk mass with a protoplasmic germinal area.
The Embryology of Chlamydoselachus 567
Shortly after the egg enters the oviduct, fertilization, encapsulation, and segmentation
take place, followed later by gastrulation and the formation of the embryo. It is not
known at what stage in the development of the growing embryo the capsule is burst,
thrown off the yolk sac, and expelled from the uterus into the sea. But it must be long
before the embryo attains the stage shown in Figure 11, plate I. However, we are here
concerned with the early stages in which the egg is still encapsuled. These eggs occur in
two distinct forms—as ellipsoidal and as round eggs.
ELLIPSOIDAL EGGS OF THE FRILLED SHARK
This form and shape of the encapsuled egg of Chlamydoselachus seems to be the
typical one. At least, save for four round eggs portrayed by Dean, all eggs figured by all
authors are ellipsoidal. This is true even of eggs freed from their capsules. Thus Brohmer
(1909) figured without capsule an ellipsoidal egg 110 mm. long with an embryo of 75 mm.
As drawn the yolk mass is 108 x 60 mm. And Garman (1913) portrayed a shell-less egg
98 x 56 mm. with a 59mm. embryo on it. Neither figure will be reproduced here since,
lacking details, they are of no particular value in this study.
Dean figured in color (Figure 50, plate V) a shell-less ellipsoidal egg 95 x 56 mm.
with an embryo 39 mm. long. Then, among his miscellaneous Chlamydoselachus records,
I have found a water-color sketch of a 55-mm. embryo on a yolk sac measuring 122 x 69
mm. This sketch, which is rather crude, was not made by Dean and was not intended for
reproduction. The egg, from which the capsule had been removed, was taken off Okinose
(Sagami Sea) in December, 1906. The references to these eggs without capsules are
merely to show that the ellipsoidal form is the predominant one. Attention will now be
directed to the capsules of these great eggs.
As portrayed by Dean, ellipsoidal encapsuled eggs seem to be of two kinds—normal
and abnormal or at least unusual. These, as figured by him and by other investigators,
will now be studied.
NORMAL ELLIPSOIDAL ENCAPSULED EGGS
The first encapsuled egg of Chlamydoselachus ever figured may be taken as an ex-
ample of the normal egg of this type. The description and figure are from Nishikawa
(1898). His material came from seven female specimens from the Sagami Sea. These
fish contained from 3 to 12 eggs each—all ellipsoidal in form. His statement follows and
evidently has to do with eggs in very early stages since he speaks of their having blasto-
derms on them. He also had eggs of the same type with early embryos as will be now
shown. Here is Nishikawa’s description:
The egg is ellipsoidal, and varies between 65~75 mm. in its shorter diameter and [ete 124
mm. in its longer diameter, the measurements being made in physiological solution of salt (Figs.
1 & 2) [Fig. 1=Text-figure 4 herein]. It bears a stumpy excrescence at one end and a slightly
recurved flattened process, about 35 mm. long, at the other. The capsule is light brown and
transparent. The space between the capsule and the yolk sac is, in earlier stages, very in-
significant, being confined mostly to the two poles of the eggs, and is filled with the white,
which is very fluid. The yolk is of a pinkish color, and the yolk-sac is very delicate.
568 Bashford Dean Memorial Volume
This description is of a live egg just taken from the body of the mother. I have found
a very similar condition in the encapsuled intra-uterine egg of the nurse shark, Ginglymo-
stoma cirratum (Text-figure 16). Here is a thick heavy capsule enclosing the huge round
yolk with its embryo surrounded by a clear glairy fluid—evidently the counterpart of
Nishikawa’s “white”. Lining the interior of the shell and particularly noticeable at the
ends is a thicker jelly-like material which cushions the yolk as the egg rolls about in
the saddle-bag-shaped uterus of the female Ginglymostoma as she twists and turns
in avoiding enemies.
Nishakawa’s drawing (Text-figure 4) shows an ellipsoidal egg in a capsule (natural
size) 135 mm. over the processes (following the curve of the long one). The egg proper is
100 mm. long by 65 deep, with an embryo 43 mm. long on it. Attention is called to the
blunt nipple-shaped process on the left, while on the right, the capsule terminates in
a finger-like curved process about 40 mm. long over its outer curve. The capsule is trans-
parent and here drawn to show the embryo and its circulatory system, but on the lower
side just inside the heavy line representing the capsule is a light line portraying the
raphe of the capsule. This extends from the end of the short blunt process along the shell
and out on the long curved process. This raphe is bilateral—the other half being found
on the side of the egg away from the observer.
Dean’s drawings of encapsuled eggs number eight, including the wind egg previously
referred to. These figures portray ellipsoidal eggs of two kinds: normal eggs with a blunt
nipple-shaped process at one end and a long curved finger-like process at the other; and
abnormal or at least unusually long eggs having at one end a long process with tendrils.
There are also four drawings of round eggs. The normal ellipsoidal eggs will be studied
first, the unusual types will later be considered in series.
Dean has figured two ellipsoidal eggs of the normal type. The first is shown in both
dorsal and ventral aspects in Figures 7 and 8, plate I. Careful comparison of Figure 7,
plate I, with Text-figure 4, a reproduction of Nishikawa’s Fig. 1. pl. IV, shows that
Dean’s figure is a copy of Nishikawa’s. The embryo measures 43 mm. in both; the yolk
in Dean’s figure is 65 x 100, in Nishikawa’s the same. Likewise the eggs in ventral aspect
(Figure 8, plate I, and Nishikawa’s Fig. 2, pl. IV) are identical. Nishikawa also had an
egg with a 50mm. embryo on it, but he had no drawing made of it. This however, Dean
had drawn in both dorsal and ventral aspects as may be seen in Figures 9 and 10, plate I.
Having cleared up these points, let us now return to a study of the ellipsoidal
capsules, which have been designated as normal. But first let it be said that no one else
has ever obtained or at any rate portrayed capsules such as these. Each of the capsules,
shown in Figures 7 and 9, plate I, has at the left end a rounded, blunt, nipple-shaped
process or eminence. On the right, each capsule terminates in a curved, finger-like
stumpy process, about 30 mm. long, and each curved in the same direction. In the drawing,
each egg has on its lower side a distinct raphe, whose relation to the blunt process is
obscure but which extends out onto the long curved process. The capsule of the younger
egg measures 128 mm. ina straight line, that of the older egg 143 mm.
The Embryology of Chlamydoselachus 569
UNUSUAL ELLIPSOIDAL EGGS WITH TENDRILIFORM PROCESSES
There are now to be considered certain eggs whose capsules may generally be desig-
nated as ellipsoidal but which depart rather widely from the forms studied. All bear
tendriliform processes. One is unusual in form but is by no means abnormal. However,
it does bear tendrils. Of all the unusual eggs, it departs so little from the normal that it
will be considered first in this category.
An Etuieticat Eco
This egg is elliptical rather than ellipsoidal in outline and bears tendrils at one end
(Text-figure 19). It is the only encapsuled egg, other than Nishikawa’s (Text-figure 4)
Text-figure 19
An elliptical encapsuled egg (in natural size—112 mm.) in the Museum of Com-
parative Zoology, Cambridge, Mass. Note the striae on the capsule and the
tendril-bearing process on the left. The stump on the right looks as if a similar
process had been cut off.
After Garman, 1913, Fig. 4, pl. 59.
that has ever before been portrayed asa published figure. In 1906, this egg was brought
from Japan by Dr. Thomas Barbour and deposited in the Museum of Comparative
Zoology at Cambridge, Mass. In 1913 it was figured but not described by Samuel
Garman. As my Text-figure 19 shows, the outline of this capsule is an almost perfect
ellipse. The egg measures about 90x 70mm. The total length of the capsule is 112 mm.
and of this the long process accounts for about 18 mm. At the left, the long seemingly
round process breaks up into three short unequal-sized stumps and each of these into
a number of smaller processes, of which the finer outer parts (see Figure 13, plate I) have
broken away. At the right end is the stump of a process, apparently the product of an
amputation by means of a dull knife of such a process as is still present on the left. The
shell is covered with parallel striations. The egg is so drawn that the raphe forms both
upper and lower edges or limits of the figure. Garman also figures the egg yolk with its
59-mm. embryo removed from the capsule as has been noted.
570 Bashford Dean Memorial Volume
Next for study are three ellipsoidal tendril-bearing eggs found portrayed in Dean’s
portfolio of drawings of Chlamydoselachus. These eggs are not merely ellipsoidal but are
decidedly oblong. Two of them were fertile, while the third, the wind egg previously
referred to, was infertile.
Some Ostone Fertite Eccs
In Dean’s notes, as already referred to herein, the small wind egg is recorded as
coming from the left oviduct of a female Chlamydoselachus taken off Misaki in 1905. From
the right oviduct of this same fish were obtained “3 oblong eggs” of which two were
“drawn”. The one of the oblong eggs, not drawn, was roughly sketched in pencil in the
notebook with the caption “stage early, probably gastrula”. This sketch is reproduced as
number C in my Text-figure 26. Note that the capsule has a tendril-bearing process at
oneend. This is very like the process in one of the “drawn” eggs now to be studied.
Symmetrical Oblong Eggs.—With the notes just quoted is the cryptic statement
“135 mm. x 70 and longer”. I identify the two oblong eggs “drawn” with Figures
2 and 3, plate I. The smaller egg (Figure 3) is symmetrical and measures (in the original
drawing) 116 mm. excluding the processes and 140 mm. over them; it is 78 mm. deep. At
the right end is a very short process, apparently the remains of a longer one. At the left
end isa slightly curved stumpy process, 20mm. long. Apparently the tip of this has been
broken off leaving some splinter-like fragments. Along one side is a raphe which extends
out on the long process. Its relation to the fragment of the process at the right is not
clear. The capsule is everywhere covered with close-set parallel striations. At the left
many of these striations are gathered together and extend out on the long process.
Among the Chlamydoselachus material deposited in the zoological collection of
Columbia University and loaned by Prof. McGregor for this study, is an oblong encapsul-
ed egg. This measures 108 x 71 mm.; is not only oblong but slightly asymmetrical, and
has a large raphe similar to that on the egg figured. The raphe extends froma rudimentary
blunt process at one pole of the egg over the yolk mass and out onto a short process ending
in tendriliform fragments. This tendriliform process is somewhat shorter than that in
Figure 3, plate I, and the egg is somewhat smaller. I believe, however, that this egg is the
one figured, and that the slight differences are due to shrinking after 33 years in alcohol.
In the 108-mm. oblong egg, and in two others of about the same size from Columbia
University (both having embryos), the raphes are complete. They entirely encircle
the eggs, but are better developed on one side than on the other. Their function is
not known. The color of the capsules of these preserved eggs is a light brown. A
crumpled capsule, from which egg and embryo have been removed, appears decidedly
browner than those capsules enclosing yolk masses. Possibly this difference in color
between these capsules and that of the wind egg (Figure 51, plate V) is due to their long
immersion in alcohol.
Asymmetrical Oblong Eggs-——The larger of the two oblong eggs, referred to in
Dean’s notes, is decidedly asymmetrical (Figure 2, plate I). Its length (excluding its one
process—the other, if present, is hidden) is 135 mm. and its width 87 mm. It is pre-
The Embryology of Chlamydoselachus Sif
sumably the “larger” of the two oblong eggs recorded in Dean’s notebook. Its asym-
metry is probably not the result of handling, as might be surmised, but was impressed
upon the egg while the capsule was being formed. The long curved process measures
about 30 mm. to the fork of the tendrils and these extend out about 15 mm. further. The
capsule is everywhere traversed by fine longitudinal striations which converge at the left
end and run out onto the long tendril-bearing process. The raphe, seen on the side of
the egg next the observer, is very large and heavy. It runs out on the process which is
plainly twisted to the left.
In the Dean collection of frilled-shark material in the Department of Zoology at
Columbia University is a large somewhat asymmetrical ellipsoidal egg which deserves
description. It measure 90 mm. long x 57 deep and has on it an embryo 71 mm. long.
The large yolk mass has become split open by the action of the preservative and the result-
ing expansion has split the capsule along that raphe near to and somewhat parallel with
the body of the embryo. At the end of the egg near the tail of the little fish I can find no
evidence of a process. At the other end near the head of the fish is a process (broken off
from the capsule) which, as hardened by the preservative, is quite flattened.
This process is shown in Figure 13, plate I. In nature, the basal part is about 17 mm.
long and about 8 mm. wide. Each of its outer edges is constituted of the end of a raphe.
Between these raphe-formed edges, in the flat body of the process, about seven horny
strands can be made out with the.aid of a magnifying glass. This process is very like that
on the egg shown in Figure 2, plate I. The outer end of the process is split in two and
each half breaks up into a twisted mass of fine tendrils. Here as in Figure 2, plate I, the
raphes form a part of the tendril mass, exactly as they do in the egg cases of certain skates
and European small sharks (“dogfishes”’).
In the first plate of Dean’s figures is a separate drawing (Figure 14, plate I) which
shows such a very much frayed-out process. This process seems also to be flat and to have
the raphes forming its outer edges. It breaks up into one large and three small tendril
masses. The larger at the base seems to be constituted of about 10 string-like bodies.
The other three tendrils are separate and grade in size from outside in, the innermost
being the smallest. The larger tendril mass seems to have had a filament cut off at the
second bend, one tendril only remaining. Of the three others the median one seems to be
broken up into two. The outer and inner tendrils are of about the same length. All are
much crumpled. It seems not improbable that this drawing was made from such a process
as that described in the preceding paragraph. Since the striae run onto the processes, one
wonders what part they play in the formation of the strands in the process and of the
tendrils. One wishes for fresh material here.
An Etoncate Inrertice (Winp) Eco
Last of all of Dean’s drawings of elongate eggs is the wind egg portrayed in color in
Figure 51, plate V. It is hardly ellipsoidal but it is elongate and it has a long tendril-
bearing process as may be seen in the figure. It was presumably drawn in natural size.
572 Bashford Dean Memorial Volume
Its width is 23 mm. and its length over the processes (but excluding the tendrils) is 102
mm. At the larger end is a conical process. The long pointed end of the capsule breaks
up into a group of tendrils measuring about 10 mm. The surface of the capsule exhibits
very fine striations. Very clear is the longitudinal ridge or raphe extending from the
tendrils along the small end of the egg capsule to and across the base of the conical process.
Not visible is the corresponding one on the other side. At the lower side of the larger
end of the capsule is a clearly delimited pale area. What it is I do not know. This egg
apparently contained no yolk whatever and hence it is called “wind egg”. The color as
shown in the figure is presumably that common to all egg capsules.
ROUND EGGS OF THE FRILLED SHARK
Last among Dean’s materials for the study of encapsuled eggs are three drawings of
round eggs reproduced as Figures 4, 5, and 6 of plate I. These are labelled C, B, and A
on the drawings, and are listed in this order in Dean’s notebook in his writing, as indi-
cating their progressive stages of development. Each egg capsule is round and has short
curved processes. These eggs will be considered here in the order of size.
Egg A (Figure 6, plate I) in the original drawing measures 129 mm. over the processes,
and the diameters of its yolk mass are c. 88 mm. in the line of the processes x 87 wide.
Of the three eggs, its processes are the longest and slenderest, are of about the same size
and length, and are curved in the same direction. Egg B (Figure 5) is 115 mm. over the
processes, and its diameters are c. 87 x 96. Its processes are short and stumpy, are of
about equal size, but are twisted in opposite directions. Egg C (Figure 4) is 116 mm. over
the processes, and its diameters are c. 90 x 89. Its stumpy processes are short, of unequal
size—one more than double the size of the other—but are curved in the same direction.
All these processes appear to be ““stumpy”’, but it may be that they were sharply curved
away from the artist’s line of sight and were longer than they appear in the drawings.
Those of Egg A (Figure 6) certainly recall the longer process portrayed by Nishikawa in
my Text-figure 4, and by Dean in his Figures 7 and 9, plate I. In this respect this capsule
approaches what has been taken as the normal type.
In the capsule of each egg the raphe extends across the germinal region, where it is
drawn much wider. It runs out onto and helps form each process. The striae are not
visible over the egg but show faintly at the poles, where they converge and extend out
on the processes. The formation of these processes is not easy to understand and so far
as I know has never been explained. The anterior process of the capsule must be formed
in the lower outlet of the shell gland while the egg in the shell gland is having its capsule
laid down. As I shall show later the posterior process is formed as and when the en-
capsuled egg passes out of the gland on its way to the uterus. The exit orifice of the shell
gland is small and its sphincter muscle evidently constricts the ends of the shell while
they are still soft and gelatinous. While the processes are being formed, the striae on
them are laid down in a way not as yet understood.
The Embryology of Chlamydoselachus 573
These encapsuled round eggs have been designated “unusual” since no one save
Dean seems ever to have seen such, but they cannot be termed abnormal. Each seems to
have a late blastula on it (these will be considered later) and there is undisputable proof
that these round eggs go on to full development. This is admirably shown in Figure 11,
plate I. The young fish was 175 mm. long and it is fast toa round yolk sac which in the
original drawing measures 92 x 90 mm. and which is now freed of its capsule. Thus this
yolk, bearing this advanced embryo, has still the almost perfectly round form of the three
eggs shown in Figures 4, 5 and 6, plate I, and, judging by the sizes of these three other
round eggs, it has decreased but little in bulk.
SIZES OF EGGS OF CHLAMYDOSELACHUS
COMPARED WITH THOSE OF OTHER SHARKS
From his studies of all these extraordinarily large encapsuled eggs of Chlamydo-
selachus, Dean drew certain general conclusions as to their size and phylogenetic origin.
These conclusions are contained in the only description (a single paragraph) of the eggs of
the frilled shark which he ever published (1903). From this, I excerpt the following:
‘“Chlamydoselachus has specialized in the line of producing large eggs, the largest indeed
among recent animals, ostrich hardly excepted [egg 150 mm., 5.9 in., in long diameter |;
that it was, however, until recently an egg-depositing shark is apparent from the character
of the horn-like capsule (with rudimentary tendrilform processes) which the egg still
retains”.
At the time that Dean wrote, the egg of Chlamydoselachus was the largest egg
known to him save only that of the ostrich, but since his day larger shark eggs have been
discovered. Larger eggs are now known to be carried by various sharks of the family
Isuridae, and by the ovoviviparous nurse shark, Ginglymostoma cirratum, often referred
to earlier in this article. The eggs of these sharks will now be described that the reader
by comparisons may see how large the eggs of Chlamydoselachus really are.
SIZES OF EGGS AND EMBRYOS OF THE FRILLED SHARK
As a basis for comparing the size of the egg of the frilled shark with that of other
sharks, it will be necessary to establish the size of this egg. Our earliest information
comes from Nishikawa (1898) who had eggs ranging from 102 to 124 mm. in long and
from 65 to 75 mm. in short diameter. He also speaks of eggs “110-120 mm. long”. These
measurements were presumably made over the egg capsule and its processes. His one
figured egg (Text-figure 4) thus measured is 128 x 65 mm., but the yolk mass is only 100 x
65 mm. natural size.
Let us now turn to Dean’s materials. The three round eggs (yolks only) measure
90 x 87 mm., 96 x 87, and 97 x 88 in the original drawings. His two oblong eggs (yolks
only) measure 119 x 80, and 138 x 90. Of his other material, Figure 9, plate I, portrays
a 50-mm. embryo on a yolk measuring 108x 68mm. Then his Figure 11, plate I shows a
large embryo on a yolk sac 92 x 90 mm. Also Dean records an embryo of 331 mm. on
a yolk 111x100 mm. And finally there is the huge embryo of 390 mm. (15.35 in.)
574 Bashford Dean Memorial Volume
ona yolk measuring 100 x 70 mm. This is portrayed in color in Figure 49, plate V.
All these measurements are of the original drawings.
When one considers these measurements of such huge eggs as had never before been
recorded of any animal marine or terrestrial (save only the ostrich), it is no wonder that
Dean wrote (1903, p. 487) that ‘““Chlamydoselachus has specialized in the line of producing
large eggs, the largest indeed among recent animals, ostrich hardly excepted”. But we
will consider some eggs that exceed even the very large ones of Chlamydoselachus.
SIZES OF EGGS AND EMBRYOS OF ISURID SHARKS
Interestingly enough at about the very time that Dean was collecting adult speci-
mens of Chlamydoselachus and studying their eggs in the Sagami Sea, Franz Doflein
was also making very extensive collections of marine fauna from the same waters. He
either collected or at any rate saw specimens of the frilled shark, for in his book (1906, p.
257) he figures a male specimen—the best portrayal (Text-figure 5 herein) yet published
of the male fish. He also obtained a huge shark egg and later described it in the follow-
ing terms:
The eggs of a giant shark were to me one of my most surprising discoveries. I had often
gotten these eggs from the fishermen but I never obtained the mother fish. They were,
however, taken from the mother fish, which evidently belongs to the viviparous sharks.
_ With their enormous yolks, they seem to be the largest eggs yet known from the animals of
that.region. They were considerably larger than ostrich eggs [150 mm. long]. One could
tell them from the eggs of other sharks by the fact that the embryo was not connected with
the yolk sac by a long, ribbon-like umbilical cord, but grew directly from it.
When I had read thus far, I strongly conjectured that these were eggs of Chlamydo-
selachus, particularly since they came from a viviparous shark and since Doflein knew and
figured Chlamydoselachus in his book. But fortunately, on the page following the para-
graph quoted, Doflein figured one of these eggs and embryos. It is plainly a young Isurid
shark, and the statement is added that the yolk sac has a (long?) diameter of 220mm. No
size is recorded for the little shark, but it is still comparatively young, probably not more
than one-quarter grown.
Doflein brought back to Germany two of these huge Isurid uterine eggs along with
his other Japanese fish collections. These eggs and embryos were turned over to Johannes
Lohberger who made a thorough study of their external morphology and internal anatomy
(1910). He found that the larger and older embryo (Text-figure 20 herein), after being in
preservative for four years, was 553 mm. long (21.8 in.) and 63 mm. wide where it rested
on the yolk mass. The length of the yolk mass was 211 mm. (8.3 in.) and its transverse
diameter 123 mm. (4.85 in.). The weight of embryo and yolk was 2.68 kg.=5.9 lbs.
The size of the female Lamna from which embryo and eggs were taken is not given and
probably was not obtained.
In the same year that Lohberger published on his Lamnid embryos from Japan,
Shann (1910) described embryos of Lamna cornubica from Scottish waters. He
quotes H. C. Williamson that the largest porbeagle embryo he had ever seen was “19
inches in total length . . . the yolk measuring 9.25 inches in length”. Shann’s description
The Embryology of Chlamydoselachus 575
and table of measurements of his own four embryos are so involved that I can make out
little about them. He had four embryos measuring 10.25, 18, 18.5 and 24 inches respec-
tively and all in about the same stage of development. His detailed yolk-sac measurements
are unintelligible to me—one wishes for diameters such as those given above. Shann
states that one of the largest embryos he examined “was a female measuring 21.75 inches
and the yolk sac was still of enormous bulk”. This is confirmed by his roughly-drawn
Text-figure 20
Egg and embryo of an Isurid shark (Lamna sp.) obtained in the Sagami Bay by Franz Doflein
c.1905. The embryo was 553 mm. (21.8 in.) long. The yolk sac measured 211 mm. (8.3 in.)x 123 mm.
(4.8 in). The whole weighed 2.68 kg. =5.9 lbs.
After Lohberger, 1910, Fig. 1, pl. I.
figure which shows that the word “enormous” is correctly used. The yolk reaches almost
from the angle of the jaw to the base of the caudal fin. He judges that at birth the young
fish would be approximately 30 inches from tip to tip.
Other Isurids have large embryos on huge yolk sacs. Two cases will be indicated.
Sanzo (1912) figures and describes from the Mediterranean the intra-uterine embryo of
Carcharodon rondeletii, the great white shark or “man-eater”. The embryo was 361 mm.
576 Bashford Dean Memorial Volume
(14.2 in.) long but no dimensions of the elongate yolk sac are given. The specimen weigh-
ed 800 g. (28.2 oz.) of which the yolk alone weighed 500 g. (17.9 oz.) In his figure the long
yolk mass extends from the pectorals to beyond the cloaca.
Since the above was written, I find that, unknown to Dean, Lohberger, Shann,
Sanzo and myself, a far larger egg and embryo of another Isurid shark had been recorded by
Vaillant in 1889. He described but unfortunately did not figure an embryo of Oxyrhina
spallanzanii whose total length was “50 cmt.”* (500 mm., 19.65 in.) ona yolk sac measuring
235 x 140 mm. (9.25 x 5.5 in.). Fish and yolk had been more than 50 years in alcohol.
Yet, “Le poids total de cette piéce, qui répresente en somme un oeuf gigantesque de
Selacien, est, dans état actuel de conservation, de 3 kil. 250 gr.” This weight (3250 g.,
114.6 oz., 7.2 lbs.) seems incredible hence I have quoted Vaillant verbatim. So far as
I know this is the largest egg and embryo of any shark ever described.
I can not find that the egg capsule of an Isurid shark has ever been figured. Not
only does one wish to see an embryo and yolk sac of one of these sharks for comparison
with a like stage of Chlamydoselachus, but also for comparison one wishes to see and
examine the capsules which enclose the largest eggs in the animal kingdom—eggs much
larger than those of the ostrich.
There is in the Museum collection an egg and embryo of Chlamydoselachus mounted
for display on a sheet of glass in a rectangular jar of alcohol. The embryo measures 370
mm. (14.55 in.) and the yolk sac 78x 60mm. Dismounted, and with the excess of alcohol
drained off, egg and embryo weigh 213 g. (7.5 oz.) Another yolk sac of about the same
size (74 x 60) detached from its embryo weighed 142 g. (5 0z.) The little fish, drawn when
fresh (Figure 49, plate V), measured 390 mm. and the unhardened yolk 100 x 70 mm., but
after being in alcohol for at least 33 years it has shrunk to the dimensions noted above.
The weight has also decreased somewhat. There is much yellow oil in the yolk. This
soaks out into the alcohol, which has periodically to be replaced by fresh alcohol.
This automatically reduces the weight of the yolk.
The young frilled shark is a little longer (370 vs. 361 mm.) but much more slightly
built, especially in the forward parts, than Sanzo’s Carcharodon. The total weights are
very different—213 vs. 800 g.; but after all the greatest difference is in the weight of the
yolk sac—142 vs. 500 g. Here contrast Dean’s Chlamydoselachus (Figure 49, plate V)
with Lohberger’s Lamna (Text-figure 20).
SIZES OF EGGS OF THE NURSE SHARK
I have unfortunately never seen the eggs and embryos of Lamna nor Carcharodon
but I have studied the encapsuled eggs and early embryos of the nurse shark, Gingly-
mostoma. And since these heavy-shelled intra-oviducal eggs are in many ways similar
to those of Chlamydoselachus, some data concerning them in the encapsuled stage will be
valuable here for comparison. My figures give lengths and unfortunately girths instead of
widths of the capsules. Furthermore since it was not easy to measure the horizontal
diameter of the yolk mass through the thick and oftentimes scarcely transparent capsule,
The Embryology of Chlamydoselachus Hi)
I mistakenly did not record the measurements of the yolks. Since the capsules are not
round but flattened dorsoventrally, it would have been difficult to get measurements in
this dimension.
In my notes I have measurements of 5 wind eggs recorded as “infertile”. These are
105 mm. long x 120 in circumference; 105 x 145, 116 x 110, 122 x 145; and 130 x 146 mm.
I noted the measurements of 6 average-sized fertile eggs as follows: 133 mm. long x 185
in circumference; 134 x 192; 141 x 185 (2 capsules); 142 x 193; 150 x 190—average 140
long x 187 in girth. From this it is seen that there is considerable variation in size—tess
in girth than in length. The girth of the capsule is pretty constant because the size of the
contained yolk mass is fairly uniform. The variation in length is mainly due to variations
in form and shape in the posterior or last-formed end of the capsule. This is sometimes
pointed and sometimes blunt but always seemingly “pinched together”. The anterior or
first-formed end looks “‘finished”, the posterior end, the last to emerge from the shell
gland, looks unfinished. For these points see Text-figure 16. This matter of the posterior
or unfinished end of the capsule will be referred to later.
It was difficult to get the weight of the yolk. This is surrounded by a clear glairy
fluid which slowly flows like thick syrup. Next to the shell this becomes a thick jelly
which adheres to the shell. At the ends of the shell this jelly forms the “plugs” already
noted—see Text-figure 16. These substances—glairy fluid and jelly—probably corre-
spond to the “white” of Nishikawa. To get at the weight of the yolk, shell and contents
were weighed. Then a window was cut in the upper part of the shell, and the yolk and
some of the surrounding glairy matter were poured out. The shell, the jelly and the re-
maining glairy material were then weighed. The data for my two largest eggs are as
follows. Egg 1, 180 mm. long x 220 mm. in girth, weighed 318 g. The shell and jelly
weighed 64 g. and the yolk 254 g. Egg. no. 2 was about the same size (no figures recorded)
and weighed 311 g. The shell and jelly weighed 56 g. and the yolk 255 g.
From the data set out above, and from the eggs and capsules shown in Text-figures
16 and 21 it is manifest that, while the encapsuled egg of Ginglymostoma is very large, it
is not so large as that of Lamna or Carcharodon. The average for the 6 normal-sized eggs of
Ginglymostoma is 140 mm. (5.5 in.) long x 187 (7.4 in.) in girth. These eggs are somewhat
flattened and have thick heavy raphes on each side. These help increase the girth measure-
ments. Text-figure 16 was made from a large and entirely normal encapsuled egg. Its life
size was unfortunately not noted, but as shown in the text-figure, it has been reproduced
140 mm. in length—the average as worked out above. This is just slightly more than the
natural size of the encapsuled egg of Ginglymostoma figured by Garman (1913, Fig. 3, pl.
59). From these data it is seen that in size of their eggs these sharks rank thus; Chlamy-
doselachus has the smallest, Ginglymostoma the intermediate-sized, and the Isurids the
largest eggs.
Again must comparison be drawn between the body size of Chlamydoselachus and
that of these other sharks. The frilled shark has an elongate slender body averaging c.
578 Bashford Dean Memorial Volume
5.1 ft. (largest 6.4 ft.)—-with a correspondingly small abdomen (Text-figures 5 and 7).
Yet in its right uterus it may carry as many as 7-12 large eggs and embryos. On the other
hand, the nurse shark is large (average adult about 8 ft. long), broad and somewhat flat,
and has a large abdominal cavity. Both of its uteri are functional and at breeding season
become enlarged into a pair of saddlebag-like organs each of which may contain as many
as 21 of the large eggs portrayed in Text-figure 16. The porbeagle isa fairly large shark.
Shann notes females from 5-9 ft. long—more of the smaller size being recorded. I have
no data for the size of the body cavity, but it must be large to accommodate the eggs and
embryos noted above. Both uteri of Lamna are functional. Three and occasionally four
young are produced, but one on each side, or one on one side and two on the other are
more common. The young at birth are probably 28-31 in. long, and, since these young
sharks are very large forward, they must fill the uteri and the abdominal cavity quite full.
But to sum up, it can be said with assurance that the evidence points to the belief that
in proportion to the size of its body cavity, the frilled shark ripens and incubates the largest
eggs known at this writing.
With the making of these historical notes a part of the record dealing with the size of
the encapsuled eggs of Chlamydoselachus, we will now turn to the study of the formation
of the capsule.
FORMATION OF THE EGG CAPSULES
OF CHLAMYDOSELACHUS AND OF GINGLYMOSTOMA
The presence of the thick keratinoid shell about the egg of an ovoviviparous shark is
surely an archaic feature. As Dean long ago (1903) pointed out, this is a heritage from its
egg-laying ancestors. Now all egg-laying elasmobranchs known to me have on their
shells tendrils or holdfasts which catch on seaweed, stones, and other objects. Thus
anchored, shell and egg escape being rolled about and injured or covered with sand or
silt, and are assured of fresh water and oxygen.
As in other sharks, so in Chlamydoselachus these capsules are secreted by the shell
gland, the interior of which is shown in Text-figure 13. For a description of this gland
see page 550. As I have pointed out earlier, the egg shell exhibits minute striae, which
sometimes have a faint spiral arrangement, and which in all cases are gathered up and
extend out on the processes. For these see Figures 2 and 3, plate I. These striae are
undoubtedly impressed on the capsule during its formation. The peculiar internal
structure of the shell gland seen in Text-figure 13 must be responsible for these. The shell
gland is somewhat flattened in form and I judge that the raphes are formed at the sides
where the dorsal and ventral inner surfaces of the gland are united. The structure of the
shell gland in Chlamydoselachus has yet to be thoroughly described and the details of its
function explained.
Excepting only the round eggs portrayed by Dean, all egg capsules of the frilled
shark figured have a long functional process at one end of the capsule. In most of the
other eggs portrayed, the other end of the capsule has a low conical blunt nipple-like
The Embryology of Chlamydoselachus 579
process—as figured by Nishikawa (my Text-figure 4); and by Dean, Figures 7 and 9,
plate I. Or this is very blunt and looks cut off as shown by Garman inText-figure 19. Or,
at this end of the capsule, the process is almost or entirely lacking as seen in Figures 2
and 3, plate I, and as found in eggs deposited by Dean in the zoological museum of Colum-
bia University. Thus one end of the capsule looks “finished” and the other—especially
when the process breaks up into tendrils—tlooks decidedly unfinished. However, the
practical disappearance of the process at one end of the capsule, taken in connection with
the fact of uterine gestation of the egg, is surely indicative of an evolutionary movement to
get rid of the capsule around the egg of Chlamydoselachus.
Nothing is known as to the method of formation of the capsule and its processes in
Chlamydoselachus. This could only be had by dissection of females immediately after
capture in the hope of finding capsules still in the glands. How improbable is such an
opportunity, the reader will readily realize from considering the habitat of the fish and the
difficulty of its capture. However, I have fortunately been able to make such dissections
and observations on the nurse shark, Ginglymostoma cirratum, which, as noted, carries
in each uterus eggs with large thick-walled blunt-ended capsules. In this capsule, one
end is likely to be smaller and seemingly pinched together, more “‘finished”, like that of
Chlamydoselachus, while the other is larger, somewhat drawn out and blunter, unfinished
looking—this end being presumably that last formed. In Text-figure 16 one cannot make
this distinction very readily, because the ends are very much alike. But since I have
examined scores of these eggs, I am satisfied that the longer and broader end of the capsule
is the younger. Furthermore, the blunter end is plainly the younger in the eggs shown in
Text-figure 21. Then there is another criterion on which to base judgment. The egg
(yolk mass) is placed excentrically in the shell (Text-figures 16 and 21). This results from
the fact that the jelly-like substance lining the shell forms a larger plug in one end of the
capsule. In these unequal-ended capsules of the nurse shark, this larger amount of jelly
is in the “unfinished” or younger end as may be seen in the figures referred to.
Now it is clear that Ginglymostoma is the last of a line of oviparous sharks, and that
like Chlamydoselachus, it is an ovoviviparous selachian well on the way toward a vivipa-
rous mode of reproduction. As such, Ginglymostoma like Chlamydoselachus might be
expected occasionally to retain tendrils at the larger, blunter, younger, or “unfinished”
end of its capsule. That it does this is shown in Text-figure 21. Furthermore, while at
Tortugas in 1912, I fortunately by dissection learned how and when these tendrils are
formed. The facts as ascertained will now be given from my notes.
FORMATION OF TENDRILIFORM PROCESSES
On June 16, 1913, I dissected several female specimens of Ginglymostoma and found
that “No. I fish had in the section of the left oviduct just behind the shell gland an egg
whose backward [really its anterior] end was covered with a hard tough shell (like any of
the eggs in the uterus) with the short blunted base of the absent horns drawn toward each
other, as may be seen in Garman’s drawing (1913, Fig. 5, pl. 59). The posterior end of the
580 Bashford Dean Memorial Volume
shell, however, still projected into the hinder part of the shell gland, and when drawn out
this was found to be soft and gelatinous with prolongations which were evidently tendrils
in the process of making. These were broken off in removing the egg, but they were
placed in their normal position as shown in the photograph reproduced as Text-figure 21.
This egg was “non-fertile”’.
From another female dissected on this day, I got an egg capsule with a pair of pro-
cesses 55 mm. long, and on another capsule one process 120 mm. long. These eggs were
undersized and probably infertile—though this unfortunately was not specifically noted
as it was for other eggs below standard limits of size. My notes record five other cases
from specimens dissected June 19. Some shells had processes on the posterior (i.e. last
formed) end, a few had them on the anterior (first-formed) end,
though here the capsule was generally “blunt” or rounded. The
posterior end of the capsule still in the shell gland or just out of it
was always soft, light in color and often translucent. That end
first formed and first out of the gland, the anterior end, was
always hard, dark in color, and noted as “‘finished”. These in-
fertile eggs were plainly wind eggs comparable to that of Chlamy-
doselachus shown in Figure 51, plate V.
From these facts the only conclusion
that can be drawn is that in Gingly-
mostoma the formation of these rudiment-
ary and very variable processes indicates
that they are vestigial structures inherited
from oviparous ancestors whose egg shells
had tendrils for holdfasts. Everything
points to the face that the ovoviviparous
shark Ginglymostoma is on its way toward
becoming a truly viviparous one.
No dissections and no direct obser-
vations of the formation of the egg capsule
of Chlamydoselachus have ever been made.
But several scientific men on being asked
which end of the egg capsule of the frilled
shark was finished first (was the older)
have unhesitatingly answered “the blunt
end”, and when asked why have answered
Text-figure 21
Two typical egg capsules of the nurse shark
The first, a wind egg,
has the rudiments of tendrils at the hinder end.
The second, a fertile egg, has the normal, blunt,
unfinished hinder end to its capsule.
Photograph by E. W. Gudger.
Ginglymostoma cirratum.
that “It looks finished’’—and so it does,
while the end having the process looks
‘“unfinished”’. For these points contrast
the two ends of the capsule in Nishikawa’s
egg (my Text-figure 4) and in Deans’
The Embryology of Chlamydoselachus 581
drawings (Figures 7 and 9, plate I). More markedly does this contrast appear in Gar-
man’s drawing (Text-figure 19 herein) and in Dean’s two oblong eggs (Figures 2 and
3, plate I).
Not being able to decide by observation which is the anterior or older end of the
egg capsule in Chlamydoselachus, let us turn for comparison and explanation to the very
similar egg shell of the nurse shark, Ginglymostoma, in which I have settled the matter
by dissection and direct study. My observations on the formation of the process of the
egg shell of Ginglymostoma make clear when and how the long processes seen on the cap-
sule of Chlamydoselachus are formed. Here let the reader note the twisted processes in
the figures just referred to, and the tendriliform holdfast organs seen on Garman’s egg
and on Dean’s oblong specimens. The bluntly conical, the “‘finished” end, is the anterior,
the older, the first formed; the twisted and the tendrilform ends are the younger, posterior,
or later formed. So also one can understand the formation of the very much frayed-out
tendril-bearing tips shown in Figures 13 and 14, plate I. The finished ends of the capsules
plainly came through the shell gland first and quickly, while the tendriliform ends came
last of all, lingered and were then formed.
It is diffcult to explain the formation of the three round egg cases and their short
blunt processes at each end as portrayed in Plate I. However, the smaller process of the
egg in Figure 6 was probably formed last. It seems likely that, in some way not clearly
understood, each end of a round capsule, as it passed through the sphincter at the hinder
part of the shell gland, remained in the orifice the same length of time and received the
same treatment. And asa result the two processes of each capsule are practically identi
cal. It would seem that had these eggs at the close of shell formation lingered in passing
through the sphincter the posterior process would have become long-drawn-out as seen
in the oblong capsules and as observed by me in process of formation in the nurse shark.
Thus the structure of the posterior or last-formed end of the egg capsule of Gingly-
mostoma with its abortive tendril-like processes, affords a clue to and explanation of the
formation not only of the curved finger-like process on the normal egg capsules of Chlamy-
doselachus but also of the aberrant tendriliform ones of the atypical egg shells.
EXTERNAL EMBRYONIC DEVELOPMENT
OF CHLAMYDOSELACHUS
In earlier parts of this paper I have discussed the breeding habits and have described
the reproductive organs of the frilled shark. These sections are based on Dean’s scattered
but invaluable notes and upon the scanty literature. These studies have considerably
extended our knowledge of the reproductive activities of this shark and have laid a founda-
tion for a study of its external embryonic development. For this there is at hand practical-
ly nothing but the excellent drawings reproduced in the plates. In the almost complete
absence of notes, all that can be done is to arrange the drawings in the order of develop-
ment of the embryos and to describe these as accurately as possible, always comparing
582 Bashford Dean Memorial Volume
each stage with the one just preceding it and noting the progress in development of
various organs. Here I must acknowledge my indebtedness to Scammon’s excellent work
published in 1911.
EARLY DEVELOPMENT
Since the total number of gravid females (26) obtained by Dean was not large, it is
not surprising that he secured very few fertilized eggs in early stages of development.
None of these has been preserved intact, nor do I find among Dean’s materials any blasto-
derms excised from the eggs and preserved in toto—either mounted or unmounted. My
only information concerning this material has been derived from a few scattered notes,
a small number of serial sections, and a few drawings—some ina more or less finished
condition, others mere sketches.
BLASTULAE
Nishikawa (1898) is the only student of the frilled shark who has published any
observations on eggs with early blastoderms. He states that “The blastoderm has a yel-
lowish red color, as in other sharks. The earliest stage that I have been able to obtain
was nearly circular in form and had a diameter of 1.3 mm”. This is confirmed by my
observations on the eggs of Ginglymostoma. The blastoderms were noted in 1912 as
‘‘yellow spots”, always placed “asymmetrically on the egg, generally in the corners so to
speak”. In 1914 my notes read—*Blastoderms very small, even minute [unfortunately
they were not measured], placed excentrically; in one lot of eggs from one female, 7 at
one end, and one on one side of egg’. These blastoderms in Ginglymostoma were so
small that I found them only by their color. But when removed and placed under the
microscope I could make out the cells.
This colored spot seems to be a characteristic feature of the eggs of the Elasmo-
branchii. Leydig (1852) was, so far as I know, the first to figure and describe the “orange-
yellow spot” on an elasmobranch egg. On the egg of Pristiurus melanostomum, he found
it at the end of the egg next to the rounded end of the capsule—i.e., that with short horns,
the finished or older end of the egg shell of this oviparous fish. It measured c. 3.2 mm. in
diameter. Balfour (1885, p. 222) also found this spot on the eggs of Pristiurus, on the ova
of two species of Scyllium, and on the eggs of Raja sp. He states that these blastoderms
were asymmetrically placed on the eggs of Pristiurus and Scyllium. Haswell (1897, p. 97)
found the yellow spot at the broader (older) end of the egg shell of Heterodontus philippi
of Australia. Dean shows this spot in his plates of the development of Heterodontus
japonicus, which will illustrate Article VIII of this Volume Haswell, in his preliminary
report on the development of Heterodontus philippi (1897), says ““The blastoderm in its
earlier stages, appears to the naked eye, as in other Elasmobranchs, as a circular reddish
orange spot around which is a narrow light yellow band. When this orange spot has
attained a diameter of about 2 mm. it assumes an oval shape”. Then Haswell generalized
about this spot thus—‘‘There can be little doubt . . . that the ‘orange spot’, which forms
such a striking feature of the egg of an Elasmobranch in its early stages, has been handed
The Embryology of Chlamydoselachus 583
down with little change from Palaeozoic times”. It is interesting to note the occurrence
of this spot on the egg of that shark (Chlamydoselachus) to which systematists have as-
signed the lowest rank among recent elasmobranchs.
Nishikawa (1898) also had older blastoderms of Chlamydoselachus. He says “The
next stage was a blastula, with a distinct segmentation cavity, whose floor was bounded
by what has been termed ‘periblast’ with fine granular yolk, and merocytes with vacuo-
lated protoplasm, due perhaps to the dissolution of the contained oil drops, and many
nuclei. One end of the blastula was thicker than the other, and is evidently the ‘em-
bryonic end’ of Balfour, and the ‘anterior end’ of Ruckert”’. Unfortunately Nishikawa
does not figure the blastoderm on the yolk, nor the entire blastoderm either in surface or
sectional view, nor does he give the size to which it has grown. It is greatly to be re-
gretted that Nishikawa did so little with this precious early material.
Text-figure 22
Diagrammatic sketches representing the
cleavage pattern in four different types of A
vertebrate eggs: A, probably a hypo-
thetical type ancestral to elasmobranchs;
B, Chlamydoselachus; C, sharks; and D, —
a type reverting from the meroblastic to
the holoblastic condition. Howey
Sketches by Bashford Dean.
In Dean’s notebook labelled CHtamyrposeLacuus there are in various places
notes on eggs and embryos obtained during his two visits to Japan, or collected after
each visit and sent to him in America. One paragraph is labelled “Material and
List of Figures’. Here I find **? Blastula”, and on another page “Apr 10, 3 blastulae”’.
He makes no specific mention of early blastulae—i.e., of early segmentation stages.
Whether the alleged “‘blastulae” were in early or late stages is not known since Dean had
no surface drawings made and since no preserved specimens can be found among his
materials. If he had live eggs of Chlamydoselachus, perhaps he had the same trouble in
finding early blastoderms that I had with live eggs of Ginglymostoma—i.e., that they
were so small that he overlooked them, since these yellow spots would be obscured by the
brownish-yellow capsules, as they were in Ginglymostoma by its thicker and darker
capsules. This diffculty would be increased in preserved eggs since the “white” (a thin
layer of glairy fluid) would be coagulated and some of the color of the germinal area would
be destroyed by the preservative.
584 Bashford Dean Memorial Volume
However, on still another page of his notebook, Dean lists and briefly describes two
“‘Blastulae” one of which he states measured “44 mm.” in diameter. These were “drawn”
(Figures 4, and 6, plate I), but, since in the original drawings they measure 44 and 48 mm.
in diameter, it seems to me that they were surely not blastulae but gastrulae. As such
they will be discussed later.
As has been noted above, Dean went to Japan in 1900 particularly to get material
for the embryology of the bull-head shark, Heterodontus. He obtained a large number of
its eggs and embryos in various stages of development (including segmentation). On the
egg of this shark, Dean published a short paper (1901.2) entitled “Reminiscences of
Holoblastic Cleavage in the Egg of . . . Heterodontus japonicus”. When he unexpectedly
began to get embryological material of Chlamydoselachus, the shark assigned by sys-
tematists to the lowest position among the Elasmobranchii, Dean not unnaturally looked
for similar reminiscences in its eggs. But, neither among his notes nor finished drawings
is there any indication that he obtained eggs in early cleavage stages.
However, there is some slight evidence that Dean found something that made him
suspect the possibility of holoblastic cleavage in the eggs of Chlamydoselachus. Among
his rough pencil sketches I find a series of four diagrams comparing, in equatorial view, the
cleavage patterns in eggs of four different types (Text-figure 22). The first (A) 1s moder-
ately telolecithal but clearly holoblastic. This probably represents a hypothetical
ancestral type. The second drawing (B) is labelled ““Chlamydoselachus”. It represents
an egg with a large blastoderm (here defined as a mass of completely formed blastomeres)
from which meridional furrows extend without interruption to an imaginary line drawn
parallel to the equator and about 35° above it. If this line represents the margin of the
germinal area, as it appears to do, then the size of this area is considerably exaggerated.
Some of the meridional lines continue further, but are more or less broken. A few reach
nearly to the vegetal pole. The third drawing (C) is labelled “Sharks’—evidently
meaning typical sharks. It represents an egg with a very small blastoderm and no radial
cleavage furrows extending beyond the margin of the mass of completely formed blasto-
meres. The fourth drawing (D), like the first, is not labelled. It portrays an egg with
a small blastoderm from which many meridional furrows extend to the equator and some
beyond it. Those that extend into the lower hemisphere are represented by broken lines.
A few of these broken lines reach nearly to the vegetal pole. This drawing evidently
represents a type of cleavage reverting from the meroblastic to the holoblastic condition.
The cleavage pattern of Chlamydoselachus, as portrayed in the second drawing, bears
some resemblance to that of Cestracion as figured by Dean (1901.2).
But are the lines crossing the margin of the germinal area really cleavage furrows?
Among Dean’s records I find three pencil drawings representing in greater detail the
circular grooves shown in eggs C. B, and A (Figures 4, 5, and 6, plate I). These pencil
drawings show very numerous fine lines crossing the groove ina radial direction. Because
of the delicacy of these lines, these drawings are not suitable for-reproduction. I have
found similar lines at the margins of the germinal area in the nearly mature ovarian eggs.
The Embryology of Chlamydoselachus 585
Here, they are merely wrinkles in the very delicate vitelline membrane, probably due to
shrinkage of the yolk mass during preservation in the mixture of formalin and alcohol.
Unless examined with a lens, they might readily be mistaken for radial cleavage furrows.
Some of the lines extend halfway to the equator of the egg. I find that Scammon (1911,
Figs. 6 and 7, pl. I) shows similar radial wrinkles outside the blastoderm in early gastrula
stages of Squalus acanthias. These I take to be identical with the very fine lines in
Dean’s sketches.
The germinal area of the egg of Chlamydoselachus (as outlined by the circles in
Figures 4, 5, and 6, plate I) is unusually large. The question arises, how much of this area
is occupied by the mass of completely formed blastomeres in the late blastula or early
gastrula stages. In his description of egg C, a “blastula”’, Dean states that it (the germinal
area?) shows segmentation over its entire extent. This segmentation might include
radial furrows extending beyond the limits of the blastoderm proper. The only drawing
which gives a comprehensive picture of the cleavage pattern is the one in the phylogenetic
series (Text-figure 22), an equatorial view. In this, the blastoderm proper is not sharply
defined. It is evidently larger than that of most elasmobranchs, but decidedly smaller
than the germinal area in which it lies. Nishikawa (1898) states that the earliest stage
(a blastoderm) that he was able to obtain was nearly circular in form and had a diameter of
1.3mm. He mentionsa later blastula, but does not give its size.
It is therefore clear that the blastoderm, in the narrow sense, occupies only a small
central portion of the germinal area. If, during cleavage, the radial furrows extend to, or
beyond, the margin of the germinal area, they must be extraordiarily long. I have
mentioned the presence, in late ovarian eggs, of fine parallel wrinkles in the vitelline mem-
brane, extending in a meridional direction and simulating cleavage furrows. My ob-
servations were made on eggs in preservative for more than thirty years and I have had
no opportunity to examine eggs in the blastula stage. I do not know of any other shark,
save only Cestracion (Dean, 1901.2), in which the radial cleavage furrows extend so far
from the region of completed blastomeres.
Text-figure 23
Section through the margin of the
blastoderm of an egg of Chlamydo-
selachus in a late blastula stage.
This drawing probably represents
the thicker end of the blastoderm in
the same series used by Dean for the
drawing reproduced in my Text-
figure 24.
After Nishikawa, 1898, p. 97.
586 Bashford Dean Memorial Volume
Nishikawa (1898) states that the yolk has a pinkish color. Presumably his obser-
vations were made on fresh material. In our specimens, in various stages of development
but not including blastula and gastrula stages, the yolk is usually pale yellow but occasion-
ally some portions are very pale pink. That Dean had live eggs with pink yolk is evi-
denced by his two drawings in color—Figures 49 and 50, plate V.
Among Dean’s few Chlamydoselachus slides there are none of either whole mounts or
sections of the blastula stage. However, there is evidence that, along with the other
materials turned over to him by Nishikawa, there were sections of segmenting blasto-
derms. In one paragraph of his notebook are a number of rough outline sketches of sections
of blastulae labelled ‘‘Nishikawa’s Slides Early”. Nishikawa (1898, p. 97) portrayed
(Text-figure 23) without caption one edge of a segmenting blastoderm but never carried
his studies further. Dean had these slides and drew a number of the sections.
Among Dean’s finished drawings are two, labelled Chlamydoselachus, which show
sections through an early cleavage stage and a late blastula stage respectively. These are
reproduced as Text-figures 24 and 25. The magnifications are not given, and the slides
from which the drawings were made have been lost. There is nothing very striking
about the mode of development portrayed, since it is typically elasmobranch; but Dean
in his only publication (1903) dealing with the development of Chlamydoselachus—a brief
note—calls attention to “the great depth of the zone of yolk nuclei”. This is well shown
Text-figure 24
A section through the germinal area of a segmenting egg of Chlamydoselachus in an early blastula
stage, showing the blastoderm (at left, above) and the broad and deep zone of periblast. At the
left, about four-fifths of the lateral extent of the periblast has been trimmed off from the original
drawing; at the right, one-fourth.
Drawing by Bashford Dean.
The Embryology of Chlamydoselachus 587
Text-figure 25
Median sagittal section (?) through the blastoderm, subgerminal cavity, and periblast of an egg
of Chlamydoselachus in a late blastula stage. The zone of periblast is evidently not shown
in its entirety.
Drawing by Bashford Dean.
in the early cleavage stage represented by Text-figure 24. Judging from Text-figure 25,
the late blastula also is remarkable for the depth and breadth of the zone of yolk nuclei,
which is evidently shown incompletely. Two other drawings of a late blastula, not
reproduced, are very similar to the one shown in Text-figure 25, and were probably
made from the same set of sections. These drawings all studied together indicate that
in these early stages the extent of the germinal area is greater than the portion of it which
is cut up into blastomeres.
It is my belief that all these drawings were made by Dean. On the boards on which
they are mounted are notes in Dean’s handwriting. The minute details in which the
drawings abound are executed in Dean’s characteristic style—according to his former
students to whose attention they have been called.
The internal structure of the late blastula described by Nishikawa (1898, pp. 96-97)
is evidently similar to the one studied by Dean and portrayed in my Text-figure 25.
Indeed Dean’s drawing was probably made from Nishikawa’s blastoderm and from
a section near the one shown in Text-figure 23. Nishikawa’s description is as follows:
The next stage was a blastula, with a distinct segmentation cavity, whose floor was
bounded by what has been termed “‘periblast” with finely granular yolk, and merocytes, with
vacuolated cytoplasm, due perhaps to the dissolution of the contained oil drops, and many
nuclei. One end of the blastula was thicker than the other, and is evidently the “embryonic
end” of Balfour, and the “anterior end” of Riickert. On the surface of the blastoderm the cells
are arranged epithelially. Most cells of the blastoderm are rich in yolk granules, but at the
bottom of the blastoderm they have only a coarsely granular cytoplasm. The blastodermic
cells are added from the periphery by the merocytes with fine yolk granules, as may be seen
from cut 1 [Text-figure 23 herein] which has been composed from two consecutive sections.
I have also found a cell simply resting on the floor of the segmentation cavity; but I cannot
say for certain whether it originated from the periblast or from the blastoderm.
588 Bashford Dean Memorial Volume
Dean’s drawing (Text-figure 25) is made from a section cut parallel to the long axis
of the future embryo. I wish to call attention particularly to the slight difference in the
portrayal of the thicker margin by Dean and by Nishikawa. Dean represents the limit of
the thickened end by a smoothly curved unbroken nearly vertical line separating the
blastomeres from the region of pericytes. Nishikawa, whose drawing was made with
a higher magnification, shows one of the embryonic cells incompletely cut off from the
yolk mass (Textfigure 23). If this cell had gone on to complete separation, then
the margins of the two figures would have been almost identical.
GASTRULAE
Earliest of all, Nishikawa collected but failed to figure and describe a gastrula of the
frilled shark. Of his one egg he states—"I have also obtained a gastrula, which was oval
in form and 3 mm. in length. I have nothing special to add about it as it was like the
gastrula of any other shark”. But was it? There is so much variability about Chlamydo-
Text-figure 26
Sketches from Dean’s notebook. A and B—
““Gastrulae 2 stages; C one of “3 oblong eggs.” (O) Ss) : @
For “2 drawn”—no gastrulae shown—see Fig-
ures 2 and 3, plate I. C was never “drawn,” ‘ B ‘
though labelled “probably gastrula.”
Sketches by Bashford Dean.
selachus that one wishes for surface views and sections. To me this seemed very small for
a gastrula and at first I was inclined to think that Nishikawa was in error, that no shark
gastrula could be so small as 3 mm. in greatest diameter. But on looking up the literature
I found that Ziegler (1902, p. 117) figures a gastrula of Torpedo 2mm. long. And Scammon
(1911) portrays gastrulae of Squalus acanthias 4.2 and 4.4 mm. long. Thus both Ziegler
and Scammon give presumptive evidence that Nishikawa was correct.
On the page of Dean’s notebook headed “Material and List of Figures”, one finds this
notation, “Gastrulae 2 stages”, followed by two pencil sketches showing eggs with
relatively large circles on them like those in Figures 4, 5, and 6, plate I. I have thought it
well to reproduce these pencil sketches as Text-figure 26. Then on the page of the note-
book on which Dean described the “3 oblong eggs”, referred to later, there is a pencil
sketch of an oblong egg with an incomplete ring placed asymmetrically (Text-figure 26),
and having at the opposite end a tendril-bearing process. This egg is labelled “stage
early, probably gastrula”. Two of these “oblong eggs” were drawn and are identified
and reproduced as Figures 2 and 3, plate I. Of the oblong egg with the gastrula, un-
fortunately no finished drawing was ever made.
On still another page of the notebook referred to is the heading, “Earlier stages, 3
eggs C.B. & A.” Then follows brief descriptions of two which he thought were blastulae
and of a third which he believed to be a gastrula. Here follow his descriptions:
The Embryology of Chlamydoselachus 589
[Egg] C [Figure 4, plate I]. Blastula shown in drawing (44. mm.) round. Shows segtn.
over entire surface [of germinal area ?]—margin not good but at several places good transition
from marginal blastomeres into central bl’ms. Not possible to trace furrows far down side of
egg.
[Egg] B [Figure 5, plate I]. Bl. somewhat later than C, [germinal area 38 x 39 mm.].
Margl. blast. fine—surface blast. smaller and less conspicuous. At several points of marg.
there are certain irregular folds of which none are (surely) gastrulation erscheinungen [mani-
festations |.
[Egg] A [Figure 6, plate I]. Gastrula 44 x 48 mm.—drawn. No surface markings—
except at margins as shn. in fig. [a pencil sketch in outline sectional view accompanies this
note |—these continued sometimes over the marg. of yolk.
This is what Dean wrote and what is portrayed (half the original size) in Figures 4,
5,and 6, plate I. Egg A (the circle measuring 44x 48 mm.), Dean thought to be a gastrula.
Eggs B (circle 38 x 39 mm.) and C (circle, 44 x 44 mm.), he calls blastulae. If A, having the
largest circle, is a gastrula, then, for all that I can see from the evidence at hand, Band C
are not blastulae but gastrulae. Just here note that in C the germinal area (delimited by
a shallow circular groove) is asymmetrically placed on the yolk. This asymmetry is
like that noted for the third egg shown in Text-figure 26. Furthermore, it may be well
to recall here that this is what I have found to be the general rule in the large eggs of
Ginglymostoma.
Each egg, as represented in Figures 4, 5, and 6, plate I, has the germinal area marked
off by a faint ring apparently representing a shallow circular groove. A similar groove
bounds the margin of the germinal area in the preserved, half mature ovarian eggs examined
and described earlier in this article. It is quite likely that this groove, if present in the
living egg, would persist through cleavage and gastrula stages; or, if it is a fixation artifact,
the same conditions would produce it in these stages. Balfour (1885, p. 222) found such
grooves in living and sectioned elasmobranch eggs studied by him.
In these drawings (Figures 4, 5, and 6, plate I), the presence of the germinal area is
indicated by faint circles only slightly darker than the remainder of the upper surfaces of
the eggs. Indeed in eggs B and C, on one side the circle, as drawn, is so faint that it
disappears into the general upper surface of each egg (especially B). Take away the
circles and there would be nothing to indicate any germinal area. For another reason it
must be noted here that one side of the ring is drawn more heavily shaded than the other.
Balfour (1885, p. 225) noted this on his preserved material—*‘In sections of the germinal
disc [of Pristiwrus], the groove which separates it from the yolk is well marked on one
side, but hardly visible at the other extremity of the section”. What then did Dean’s
artist draw and how did he see anything to draw? If he drew preserved eggs, as is most
likely, he drew the thickened edges of the blastoderms in early gastrula stages, more
thickened on one edge than the other. This Balfour found as cited above and shows in
a cross section of the blastoderm. These dark parts of the circles (Figures 4, 5, 6, plate 1),
I take to be the edges of the blastoderms wherein the embryos will be found later. In
fixed eggs the thickened edges of the late blastoderms would show up more opaque than
the inner and thinner regions.
590 Bashford Dean Memorial Volume
But suppose that the artist had before him living eggs, would not the whole germinal
area have the same color? The answer to this question is I believe to be found in my
observations of living gastrula stages in the large thick-shelled intra-oviducal eggs of the
nurse shark, Ginglymostoma cirratum. On some eggs examined on July 21, 1912, I found
an orange-colored ring enclosing an area which covered one-fourth to one-third of the
upper (or visible) side of the egg. This object was more plainly seen by cutting a window
in the capsule over this colored ring and removing some of the glairy liquid surrounding
the egg. Then, when a little sublimate-acetic was dropped on it, the whole blastoderm
became visible with the beginning embryo in it. This was again seen on July 22, on an
egg from another female. From another egg I got a “Blastoderm about the size of a silver
dollar’, and on another egg “Large blastoderm partly on top and partly on side of yolk”.
Another had ““Blastoderm covering a little more than half the upper side of yolk, with one
edge dipping over the side”. On an egg examined on July 23, the “edge of the blastoderm
was a rusty orange; embryo transparent and colorless, only visible when in motion”. In
the plates of the next article of this volume—that on the embryology of Heterodontus—
will be seen the same orange-colored ring of a blastodisc embracing an area covering one-
fourth to the whole of the upper visible surface of the 55mm. egg with an embryo so
small and transparent as to be almost invisible.
Thus the early gastrula stages of eggs of Chlamydoselachus, eggs alive or dead, were
presumably seen as drawn in Figures 4, 5,and 6, plate I. If drawn alive at Misaki then the
artist saw and drew the colored edges of the late blastodiscs. If the eggs had been “fixed”,
then it must be concluded that they were in early gastrula stages before embryos had been
formed, but that as Balfour puts it “The embryonic rim is represented by a darker shading
at the edge’. Lastly it should be noted that these blastoderms in the gastrula (?) stages
shown in the figure cited cover a substantial part of the upper surface of the eggs.
Finally, it must be said that if the eggs shown in Text-figure 26 are in the gastrula
stage as Dean expressly states, then the three eggs portrayed in greater size and detail in
Figures 4, 5, and 6, plate I, are also presumably in the gastrula stage. To me the sketches
all show eggs in the same stage. Nothing in drawings or text differentiates them.
As noted at the beginning of this section, Nishikawa (1898) states that he obtained
an early gastrula. This was sectioned and the sections were in 1901 or 1902 turned over
to Dean. Among Dean’s slides in my possession are five of serial sections of an early
gastrula of Chlamydoselachus. I presume that these were sections prepared by Nishikawa
and presented to Dean. In Dean’s notebook are outline sketches made from these sections.
The plane of the sections is oblique to the axis of the forming embryo and consequently
these sections are not very favorable for study. In general the mode of development is
like that found in other elasmobranchs.
LATER DEVELOPMENT
In this study of the frilled shark, my readers and I have now come to that part which
perhaps holds the most interest since it is the most concrete—the study of the embry-
The Embryology of Chlamydoselachus 591
ology as portrayed in Dean’s drawings. This perforce must be a study of the external
development of the embryos from the smallest figured (11.5 mm.—Figure 15, plate II) to
the largest (390 mm.)—-shown in its life colors in Figure 49, plate V.
It does not lie within the scope of this article, as indicated by its title, to attempt any
consideration of the internal development. To be sure, in my account of the blastula and
gastrula stages I have included the meager information available concerning their internal
structure. But Dean left neither notes nor drawings dealing with the early formation
of the embryo and the development of organs. I have found a few serial sections of
advanced embryos, but these are in poor condition. Therefore any consideration of the
internal development would necessarily be limited to a review of previous contributions.
In his article on the anatomy of Chlamydoselachus, Smith (1937) has included references to
the scanty literature concerned with the development of organs, and has reviewed certain
topics. It will suffice here to indicate briefly, for the convenience of future investigators,
the contents of the few publications dealing with the organogeny of Chlamydoselachus.
RESUME OF RESEARCHES ON THE INTERNAL DEVELOPMENT
Rose (1895) studied the teeth of a 340mm. embryo. These teeth were not.all in
the same stage of development; therefore they afforded a graded series. Rose’s obser-
vations indicate that the three large cusps of a typical tooth develop from separate an-
lagen; teeth are formed by the union of simple denticles homologous with placoid scales.
None of the teeth studied by Rose had attained its final form.
Nishikawa (1898) figured four transverse sections through the head of a 32mm.
embryo in the region of Rathke’s and Seessel’s pouches; also a section through the “grow-
ing point” of a lateral line of the same embryo. He states that throughout the greater
part of the lateral line there is a lumen, which is slit-shaped in transverse sections, but
at the posterior extremity it is absent. In the anterior part, where the lateral nerve is in
close contact with the anlage of the lateral line, the lumen opens to the exterior at several
points. In this connection it should be stated that, as noted by various authors (Smith,
1937), in the adult the lateral line is open throughout almost its entire length.
Dean (1903) published a preliminary report on the embryology of Chlamydoselachus.
The date of this paper comes after Dean’s first visit to Japan, but before his second visit.
Since this article is very brief, and constitutes Dean’s only publication on the embryology
of Chlamydoselachus, it is here quoted in full:
In view of the archaic features in the adult, he [Dean] noted as significant in the de-
velopment of this form the great depth of the zone of yolk nuclei, the absence of external gills,
the more nearly terminal position of the anus, the relatively smaller size of the head, the
enormous spiracular cleft and the almost typically fin-fold type of limb. Chlamydoselachus
has specialized in the line of producing large eggs, the largest indeed among recent animals,
ostrich hardly excepted; that it was, however, until recently an egg-depositing shark is ap-
parent from the character of the horn-like capsule (with rudimentary tendriliform processes)
which the egg still retains.
One may query Dean’s statement concerning the absence of external gills. In Dean’s
own drawings, gillfilaments are shown projecting beyond the gillflaps throughout the
592 Bashford Dean Memorial Volume
advanced stages of embryonic development. It is probable that what Dean meant is that
these external gillflaments are merely temporary modifications of the gillfilaments
that persist in the adult; also that they are not so long as they are in other embryonic
sharks. This matter of external gills in both embryos and adults of Chlamydoselachus will
be taken up fully in a later section of this paper. Hence it need not detain us here.
In his earlier article on the origin of vertebrate limbs, Osburn (1906) briefly mentions
some features in the development of the skeleton of Chlamydoselachus. His later article
(1907) on the same subject includes a more detailed consideration of the fin skeletons and
pelvis, accompanied by some figures of these structures in a 225-mm. embryo.
Brohmer (1908) studied the excretory system of a 25-mm. young embryo of Chlamydo-
selachus. In the stage described, the pronephros is vestigial and the mesonephros is in an
early stage of development.
Ziegler (1908) studied two embryos in the same stage, each 25mm. long. His
paper deals with the organogeny, particularly in the head region, with special attention to
the “‘head cavities.” These are cavities which, in elasmobranch embryos, occur in con-
nection with mesodermal structures called “head somites,” and are regarded as detached
portions of the primitive coelomic cavity. For a further discussion see Smith, 1937, pp.
391-392. Ziegler was unable to find the anterior head cavity discovered by Platt in 1891
in certain other selachians, although he did find an anomalous cavity which he believed to
be constricted off from the mandibular head cavity. Ziegler described also the infundib-
ulum, Rathke’s pouch, and the cranial nerves (reconstructed by his pupil, Brohmer).
Brohmer (1909) described in more detail the head somites in a 25-mm. embryo of
Chlamydoselachus. Like Ziegler, he was unable to find the anterior head cavity described
by Platt. Brohmer and Ziegler agree that there is but a single premandibular head
cavity in Chlamydoselachus. Brohmer’s contribution, like Ziegler’s, includes a description
of the cranial nerves of a 25-mm. embryo.
DESCRIPTIONS OF EMBRYOS FIGURED
On that page of Dean’s notebook labelled “Material & List of Figures” is a list of
embryos to be drawn. This list has been a partial guide for this section of the present
article—partial only, because not all the embryos there listed were drawn, or if drawn
some of the figures have in the long years since been lost. Then again the list is only
partial because I find in the plates a number of figures not included in the list. Almost
every drawing has noted on it the length of the embryo drawn, but some do not. These
latter figures are rather difficult to locate in the series. Again other drawings with
lengths indicated are not on the list. In addition to Dean’s drawings of eggs and embryos,
there have been introduced in their proper places, but as text-figures, a few illustrations of
embryos described in external aspect by other authors. These fill in gaps in Dean’s
series and enable me better to show the progressive development of the external form
of the embryos.
Owing to the complete absence of descriptive notes and the almost entire absence of
material, the stages of development must be described as they are shown in the individual
The Embryology of Chlamydoselachus 593
drawings. Each figure will be compared point by point with the next younger in order to
show the relative progress in development. Then so far as possible, comparisons will be
made with embryos of Squalus acanthias of about similar size as portrayed so well in
Scammon’s ““Normal Plates” (1911).
Aw Empryo oF 11.5 MILLIMETERS
This is the smallest embryo listed and figured, It and two other small embryos
(15.5 and 20 mm.) were taken “1905 Early January.” Presumably all came from the same
mother. If so, this shows that the embryos and eggs in a given uterus may be of different
but closely related ages. This is to be expected since the eggs presumably ripen one at
a time and are discharged from the ovary singly; certainly they pass one at a time into the
oviducal funnel, are fertilized and encapsuled as they pass down into the uterus. Fertili-
zation of these shelled eggs must take place before the capsule is formed. In Ginglymostoma
I have taken segmenting eggs from the oviduct above the shell gland.
This embryo, seen in right lateral aspect, is labelled in the original drawing “Emb.
C 11. 5 mm.”, and is shown in Figures 15 and 16, plate II. Figure 15 bears the notation
“10+”, and in the original drawing it measures 121 mm. Figure 16 is drawn to larger
scale. In length this embryo corresponds to Scammon’s (1911) Fig. 24 of an 11.5-mm.
Squalus acanthias shown in his pl. II. In development the two embryos are in about the
same stage. As my Figure 15, plate II, shows, the frilled-shark embryo is attached to
the large yolk sac by a short yolk stalk. In the original drawing this has an antero-
posterior diameter of 10 mm. but in life of about 1 mm., which is the measurement for the
cord of the 11.5-mm. Squalus. This is the “umbilical cord” of Nishikawa (1898). How-
ever, this is not an umbilical cord but merely a yolk stalk. .
On the dorsum of this frilled-shark embryo (Figure 15, plate II), there is a convexity
over the gill-arch region, a concavity over and behind the vertical of the yolk stalk,
a slight convexity behind this, and a marked downward bend of the tail. The forebrain
and midbrain make an angle of approximately 90° with the main axis of the body. The
forebrain looks downward. The midbrain is delimited from the forebrain by a groove and
superficially is sharply marked off from the hindbrain. The nasal groove, having its
greatest invagination in front, is placed just below the eye. The optic cup is circular and
without trace of optic fissure. The lens is prominent and circular in outline. The mouth
is widely distended. The gill-plate is prominent, showing seven branchial grooves—the
first indistinctly. Not all the grooves appearing in this region are branchial grooves. The
second branchial groove appears to be forked, but the anterior limb is not a branchial
groove as may be seen by comparing this drawing with Figure 16 where the gill-clefts
are shown in larger scale.
The pectoral-fin rudiment is well-outlined for this early stage, and extends backward
and downward, reaching some distance back of the hinder edge of the yolk cord. The
cloacal elevation is quite prominent and in front of it is a slight swelling which I take to be
the anlage of the pelvic fin. The tail ends in a point bent sharply downward. The
V-shaped myomeres show faintly in the upper half of the trunk.
594 Bashford Dean Memorial Volume
This same specimen was stained, cleared and drawn somewhat enlarged (to 161
mm.—x 14), apparently in order that the neuromeres and myomeres might be studied and
counted. In this Figure 16, plate II, there is plainly seen between fore-and midbrain
a small rounded body which I take to be the rudiment of the epiphysis. The neuromeres
are divided into two sets of three each by a very short neuromere (?) which I do not under-
stand. The auditory vesicle is prominent, standing over the bar between the second and
third gill-clefts. From this vesicle to the end of the tail are 102 myomeres. This was
noted in pencil on the original drawing. Plainly visible are six gill-clefts, the seventh
being very faint. The heart is prominent—as is a large blood vessel, the vitelline artery,
branching off from the dorsal aorta. The cloacal eminence is very prominent, and in
front of it is a thickening which is presumably the rudiment of the pelvic fin. The fine
line bounding the entire figure represents the superficial ectoderm.
An Emaryo 15.5 mM. In Lenctu
The next drawing called for in Dean’s “Material & List of Figures” portrays an
embryo of this size in lateral aspect (Figure 17, plate II). This drawing is labelled “Emb.
B 15.5 mm.” on the drawing. This embryo agrees in length and in development very
closely with Scammon’s stage No. 26 (his pl. II), a 15-mm. Squalus. Dean’s figure is
marked “10+” but in the original drawing it measures 177 mm. From the head, the
back line slopes down toa point about over the yolk-stalk junction. Thence it runs back-
ward almost straight to a point over the cloaca, from which region the tail bends down
sharply. The forebrain together with the olfactory rudiment is prominent and is slightly
upturned. The midbrain is large and bulges forward strongly. Thus the profile of the
head of this embryo has a striking resemblance to that of a bulldog—though the parts do
not correspond. The epiphysis is indicated by a slight swelling above the forebrain and
in front of the eye. The optic cup and lens show some enlargement. The mouth still
gapes widely.
The prominent bulge in front of the yolk is due to the presence of the heart. The
pectoral fin is larger than that of the 11.5mm. embryo. On the ventral surface of the
body is a ridge, probably an evidence of the beginning of the gut. The cloacal swelling
is very marked. In front of this is a thickening, presumably the anlage of the pelvic fin.
Above the cloacal eminence, the straight dorsum slants downward as the tail. This ends
in a curious upward hook like that found on the caudal extremity of a Boston terrier
whose tail has been bobbed and the point bent upward.
In this 15.5-mm. Chlamydoselachus (Figure 17, plate II) the gill-arch region is very
prominent. Some of the gillarches appear crumpled. This crumpling is, I judge, an
artifact due to shrinkage. In the dorsal portion of the branchial region, there appear
three ridges that resemble incomplete gill-arches. Of these, the two anterior ones are
probably not gill-arches but parts of the cranium, while the third is a portion of the first
visceral arch. One notable difference between the 15.5-mm. embryonic Chlamydosel-
achus (Figure 15, plate II) and the 15mm. embryonic Squalus, shown in Scammon’s
Fig. 26, pl. II, is that the little Squalus has at least one gill-filament projecting from each
first, second and third slit, whereas these are entirely lacking in our embryo.
The Embryology of Chlamydoselachus 595
An Emsryo Measurinc 20 MILtimeTers
The next drawing called for on the “List” is of this size. It bears the notation ‘“‘Emb.
A 20 mm.” The original drawing is marked 10+ but it measures 222 mm. The
drawing represents the embryo (in lateral view) as pulling forward on the yolk sac
(Figure 18, plate II). There is fair correspondence between this embryonic Chlamydo-
selachus and Scammon’s 20.6-mm. Squalus (his Fig. 28, pl. III). Compared with the 15.5-
mm. embryonic frilled shark, the forebrain of the 20-mm. specimen is more prominent, the
midbrain has become swollen laterally and is separated from the hindbrain by a con-
striction of its lateral and (morphologically) ventral surface. The dorsal line of this
embryo, in contrast with the younger ones, runs almost straight to what is evidently the
anlage of the dorsal fin—located just behind the vertical through the cloaca. The tail
bends down sharply without, however, any upturned point as in the preceding stage.
It is more like that in the 11.5-mm. specimen (Figure 15, plate II).
Returning to the head region, attention is called to the changed olfactory anlage and
to the much enlarged eye. The mouth is somewhat less widely open than in the preceding
stage. The gill-arch region is more prominent than ever. As in the preceding stage, some
of the arches are in their lower halves sharply angled forward. There are eight distinct
gillarches with seven gill-clefts. The first visceral (the mandibular) arch forms the upper
and lower jaws (palatoquadrate and Meckel’s cartilage respectively). In the stage shown,
with wide-open mouth, the jaws are open at an angle of about 90°. The ridge immediately
behind the eye is probably not a branchial arch but a part of the cranium; likewise the
two short ridges dorsal to the one just mentioned are presumably also eminences of
the cranium.
The arch immediately behind the mandibular arch is the second visceral or the hyoid
arch. Its dorsal half, lying immediately behind the protuberance of the skull previously
mentioned, will give rise to the hyomandibular cartilage. This, in the adult, articulates
with Meckel’s cartilage at the angle of the jaw, thus helping to support the jaw. The
first branchial cleft appears to be closed ventrally. Its dorsal portion, lying immediately in
front of the dorsal segment of the hyoid arch, will become the spiracle. For the position
and relations of the spiracular canal in the adult, see Smith (1937, Text-figs. 82 and 84).
The other visceral arches (the gillarches of the adult) are quite regular in form save for
the crumpling already mentioned.
The bulge on the ventral surface of the embryo, immediately in front of the yolk
stalk, is caused by the heart. The pectoral fin has become much broader and looks to be |
almost functional in a rudimentary fashion. The pelvic fin now shows clearly. The
wart-like cloacal eminence is but little larger than that shown in the 15.5-mm. embryo.
In front of it, the pelvic fin is clearly outlined. Back of it is the rudiment of the anal fin.
The tail ends ina point sharply hooked downward. The somites are far advanced and now
have the perfected zig zag shape faintly foreshadowed in the preceding stage —15.5 mm.
(Figure 17, plate II).
Scammon’s Fig. 28, pl. I, of his 20.6:mm. Squalus is further developed than Dean’s
20mm. Chlamydoselachus. The dogfish has all the fins, the pectoral being better de-
596 Bashford Dean Memorial Volume
veloped. But most noticeable in the dogfish is a profusion of long gill-filaments coming
out of slits 1-2-3, while shorter ones are to be seen in the spiracular cleft and the fifth
slit. There is no indication of such filaments in the 20mm. Chlamydoselachus, although
the slits have apparently broken through.
Two 25-mm. SpeciMens—Heaps Onty—Descripep BY ZIEGLER AND BROHMER
In 1908, Paul von Rautenfeld brought to Germany from Japan a collection of zoologi-
cal material, among which were three embryos of the frilled shark—two of 25 mm.
without yolk sacs and one of 70 mm. with a yolk sac. These presently came to H. E.
Ziegler for study. He figured and described (1908) one 25-mm. head in both lateral and
ventral aspect. Then he cut sections of this and studied them as noted above. The
other 25mm. embryo and the 70-mm. specimen on its yolk sac, briefly referred to else-
where, were turned over to his student, Brohmer. The latter deposited the larger embryo
in the museum at Jena, but figured and described the head of the 25-mm specimen in
dorsal aspect (1909). Then he sectioned it and studied it in comparison with like em-
bryonic material from other sharks..
Dean’s embryos above were all portrayed in lateral aspect only. The head of
Ziegler’s embryo was figured in lateral and ventral views and Brohmer’s of the same size
was portrayed in dorsal view. Since nearly all Dean’s embryos figured are shown in all
three aspects dorsal, lateral and ventral—these figures will be studied in that order. For
this reason it has seemed well to begin consideration of the 25-mm. specimens by properly
combining and studying the figures of Brohmer and Ziegler.
Head in Dorsal Aspect.—First let us consider Brohmer’s figure (1909) of the head of
the 25-mm. embryo seen from above reproduced herein as Text-figure 27a. Here the
head seems to be pointed. The eyes are prominent, as are the spiracles. The gill-arches
stand out widely—the first at about right angles to the body, the other five being directed
obliquely backward. All have very short external gill-filaments. The pectoral fins show
the beginnings of the basal cartilages. The most striking thing shown in this embryo
is the transparent roof of the hindbrain—through which can be seen the floor with
its median groove.
Ziegler (1908) figured the head of one of the 25-mm. embryos in both lateral and
ventral aspects (my Text-figure 27). I will first give Ziegler’s descriptions of his figures,
and will then call attention to particular points. Ziegler wrote as follows:
Der weit gedffnete Mund ist jederseits von dem Kieferbogen begrenzt. Die Ober-
kieferwulste sind gross und lassen vorn median zwischen sich noch eine Lticke, an welche sich
eine kleine mediane Rinne an der Unterseite des Vorderkopfes anschliesst. Auffallend ist die
Grdsse des Spritzloches und die ausserordentliche Weite der ersten echten Kiemenspalte.
Die folgenden Kiemenspalten sind schmal und unter einander nicht viel verschieden. Bekannt-
lich gleicht Chlamydoselachus insofern dem Hexanchus, als 6 Kiemenspalten auf das Spritz-
loch folgen.
Hinter der letzten Kiemenspalte liegt noch ein kleiner Wulst, welcher die Kiemenregion
abschliesst; an Fig. 1 wird er durch die letzte Kiemenplatte verdeckt. Dann folgt die vorder
Extremitat, sowie ventral der Nabelstrang.
The Embryology of Chlamydoselachus 597
Text-figure 27
Heads in three aspects (dorsal, lateral, and ventral) of two 25-mm.
embryos of Chlamydoselachus.
A after Brohmer, 1909, Text-fig. 2; B and C after Ziegler, 1908, Text-figs. 1 and 2.
Head in Lateral View.—In addition to Ziegler’s brief general description of the head
of his 25mm. embryo, comparison of it in this aspect (Text-figure 278) should be made
with the head of the 20-mm. specimen in lateral view (Figure 18, plate IJ). The head of
the 25-mm. embryo is filled out and rounded with the forebrain pointing downward.
The mouth still gapes widely. Brohmer (1909, Text-fig. 3) had a drawing made of his
25-mm. embryo in lateral aspect. This in its portrayal of the anterior visceral arches
differs somewhat from Ziegler’s figure of his specimen of the same size. It is difficult to
understand the mode of development of the anterior visceral arches as portrayed in lateral
view by these two investigators. Possibly their embryos were abnormal. However, in
some ways they are related to what we shall find in Nishikawa’s 32-mm. specimen.
In Ventral Aspect.—There is no like view of the head of the 20mm. embryo
available for comparison. This is our first description of the head of an embryonic
Chlamydoselachus seen from below (Text-figure 27c). The snout-like forebrain stands
out against the background of the larger rounded midbrain. The eyes and nasal capsules
show faintly. The opening of the expanded mouth is about as broad as long. The halves
of both upper and lower jaws are separated by fossae—the upper fossa is the wider.
The gill-arches are distended, and short filaments are seen on their hinder sides. The
pectoral-fin fundament shows traces of the basal cartilages. The yolk cord is large in
comparison with the size of the body.
598 Bashford Dean Memorial Volume
Scammon’s drawing of his 24.7-mm. Squalus is in full-length lateral aspect only.
When Ziegler’s drawing of the lateral head of his 25-mm. specimen is compared with the
head only of Scammon’s Squalus, it is at once seen that the latter is more developed. Its
gill-arches are more finished and are filled witha profusion of long external filaments. The
spiracle is closed off and is also filled with filaments. Its pectoral fin, however, is in about
the same stage of development as that of Chlamydoselachus.
NisHIKAWA’s 32-mM. EmMprvo—Heap ONLY
The next stage called for in Dean’s “List of Figures” for the development of Chlamy-
doselachus, is noted thus ‘““Emb. of mm. 32—general view 2 figs.; head 3 pos’ns.” No
“general view 2 figs.” can be found, but there are views of the head only, in dorsal,
lateral, and ventral positions. These are reproduced as Figures 19, 20 and 21, plate II.
But before describing them, I wish to set forth here a very interesting matter. Earlier in
this article, I have expressed the belief that all Nishikawa’s materials were turned over to
Dean while he was working at Misaki and Tokyo. Nishikawa’s brief article had been
published in 1898 and in it he had figured the head of a 32-mm. embryo (his smallest
specimen) in dorsal, lateral and ventral aspects. Dean had no specimens of his own be-
tween 20 and 34mm. To lessen this gap in Dean’s series of drawings showing the pro-
gressive development of the frilled shark, the figures of the head of Nishikawa’s 32-mm.
embryo were redrawn at the University (by Kuwabara ?) for reproduction by lithog-
raphy. I have compared the two sets of three figures minutely and can affirm that they
are identical.
But the reader may be wondering why Dean had Nishikawa’s figures copied instead
of having drawings made de novo. and why no full-length drawings are available as called
for. The answer is to be found in Nishikawa’s article (1898, pp. 98-99) wherein he
figures diagrammatically and describes sections of the head of this enbryo—it had been
cut into sections in 1896.
Head in Dorsal Aspect.—The head of the 32mm. embryo is seen from above in
Figure 19, plate II. This head must be contrasted with that of the 25-mm. embryo por-
trayed in Text-figure 27a. The head in each figure is pointed. The curious outline on
the head in Figure 19, plate II, is probably caused by the shrinking of the skin on the
embryonic skull. In the 25-mm. head as drawn, the tissues are transparent and allow one
to see the floor of the brain cavity. The 32mm. head has the openings of the endolym-
phatic ducts which are lacking in the 25mm. head. The former has the large spiracles
seemingly placed higher on the head than those of the younger embryo. There are short
filaments on both sides of the widely spread gill arches of each head. The rudimentary
pectoral fins are about in like stages of development in each embryo. On the whole the
head of the 32-mm. specimen looks older and more perfected.
Head in Lateral View.— It is to be regretted that no full length drawing of the 32-
mm. embryo in lateral aspect is available for comparison with that of the 20-mm. specimen
(Figure 18, plate II). One wishes to see what differentiation has taken place in body and
tail as well as in the head. However, Figure 20, plate II, shows some interesting struc-
The Embryology of Chlamydoselachus 599
tures absent in the head of the 20-mm. specimen but found in the beginning stage in the
25-mm. embryo as seen in Text-figure 27..
As Figure 20, plate H, shows, this 32mm. specimen differs markedly in the head
region from the 20-mm. embryo portrayed in Figure 18. The smoothly rounded fore- and
midbrain vesicles are separated from each other by a cleft. The olfactory organ is well
established, as is the eye which on the ventral side shows a trace of the optic cleft. The
mouth is still widely open but far less so than in the 20mm. embryo (Figure 18, plate II).
The seven pairs of visceral clefts are open to the exterior and to the pharyngeal cavity,
the second being the largest and the seventh (the sixth branchial cleft) the smallest. The
first, the spiracular cleft, is almost closed off ventrally.
Further comparison of the 20- and 32-mm. specimens shows that the crumpled gill
slits of the 20mm. embryo are in the 32-mm. head replaced by the more normal straight
ones. All the clefts (including the spiracular) have external filaments in the 32-mm. head.
It is interesting to note that the ridge immediately posterior to the eye in the 20mm.
specimen together with the hinder region of the upper jaw have here developed into a very
prominent cheek-like process. The growth of this process apparently assists in the for-
mation of the hinder part of the upper jaw and of the cheek region while at the same time
superficially closing off the spiracle on its ventral side. It also assists in bringing the
posterior end of the upper jaw in closer proximity to the hyomandibular element of
the hyoid arch. :
Let us now contrast the lateral view of the 25-mm. head shown in Text-figure 278
with that of the 32-mm. specimen portrayed in Figure 20, plate I]. The 25-mm. head is
more smoothly rounded. The eye has a fissure at its hinder edge whereas the other head
has it in a ventral position. The mouth of the younger fish is more widely open. But
most unusual of all are the curious structures around the spiracular opening. These I do
not understand—possibly this specimen was abnormal. In any case these objects seem to
be forerunners of the cheek pieces of the 32mm. specimen shown so prominently in
Figure 20, plate I]. There is nothing unusual about the gillarches and clefts of the
25-mm. fish save that the first is more widely open than that of the older specimen.
Behind the seventh cleft on each head and almost over the yolk-stalk are the stubby pecto-
ral fins. Faint traces of the lateral line are seen on each specimen.
Head in Ventral Aspect.—The drawing of the ventral aspect (Figure 21, plate IJ)
gives one a clearer idea of the morphology of the organs on the sides and lower surface of
the head. Note the head, blunt-pointed in this aspect, the prominent eyes, and also the
kidney-shaped outlines of the nasal pits. The cartilages of the lower jaw have united, but
between those of the upper there is stilla gap. In the mouth behind this gap is a structure
which Nishikawa, by sectioning this head, identified as Rathke’s pouch extending back
toward the infundibulum. In contrasting the 32mm. head with that of the 25-mm.
specimen in ventral aspect, it is seen at once that the former is much older and more
“finished”. Contrast the widely gaping round mouth of the younger fish, with its two
median fossae, with the far more normal mouth of the older specimen. No further comment
600 Bashford Dean Memorial Volume
is necessary. Note that in both heads, the isthmus grows progressively narrower from
back to front. Short external filaments are found on each side of each arch.
Scammon’s stage of Squalus nearest to this 32mm. Chlamydoselachus is one of
28-mm. portrayed in full-length lateral, dorsal and ventral aspects (his Fig. 30a, b and c,
pl. III). Since there is no fulllength drawing of the 32mm. Chlamydoselachus, com-
parisons are difficult. But comparisons of heads only show that this 28mm. Squalus is
much farther developed than the 32mm. Chlamydoselachus. This is particularly true in
the gillregion. The spiracular cleft of the dogfish is finished, and from it and the other
clefts a profusion of long external gill- filaments protrude.
Dean's EMBryo 34 MM. IN LENGTH
The “List of Figures” calls for ‘““Embr. of 34 mm. Entire: head 2 other positions”.
And fortunately there are of this embryo a full-length drawing in lateral aspect (223 mm.
long in the original) shown in Figure 23, plate II, and also dorsal and ventral figures of the
head. Comparisons will be made of the head of this specimen in three aspects with
the drawings of the head of the 32mm. embryo. In addition comparison of the figure
of the 34-mm. specimen in full lateral view will be made with the similar figure of the
20-mm. embryo.
Head in Dorsal View.—As may be seen in Figure 22, plate II, the head of this
embryo contrasts strongly with that of the 32mm. specimen. It is bluntly rounded and
the eyes are less prominent. Let the reader contrast the markings on the head over the
brain in the two figures. I do not understand them unless they are due to shrinkage of
the soft tissues on the embryonic skull. Let the observer particularly note that the open-
ings of the endolymphatic ducts are no longer visible. The spiracular openings are
smaller. The gill-covers are less widely spread and in this aspect no filaments are seen in
them. The pectorals are about as they were in the 32-mm. embryo.
Lateral Aspect, Head Only.—The head in this view (Figure 23, plate II) should be
compared with the lateral view of the head of the 32mm embryo (Figure 20, plate II).
The head of the 34mm. embryo is more rounded. The eye still shows the choroid
fissure. The greatest progress however is to be noted in the mouth and spiracle. The
mouth begins to look somewhat like that of a shark. Most noticeable is the fact that the
cheek-piece so conspicuous in the 32mm. embryo (Figure 20, plate I) has here grown
fast to the hyoid arch. The external opening of the spiracle is much smaller and is in line
with the medial borders of the gillslits. The first gill-slit is very large, and its arch and
all the other arches show backward folds where they join the body above and the
isthmus below.
Head in Ventral View.—In this aspect (Figure 24, plate Il) it is noticeable that the
nasal pits are smaller. The fossa between the cartilages of the upper jaw is much reduced,
the mouth itself is less widely open than in the 32-mm. specimen (Figure 21, plate II),
and is more adult in appearance. The reduction in width of the isthmus from the region
of the sixth flap forward to the first is very noticeable. The distended first gill-covers
The Embryology of Chlamydoselachus 601
nearly meet across the isthmus, presaging the condition that suggested the name of our
fish—the cloak-gilled shark.
Lateral Aspect, Full Length.—Comparison from this viewpoint of the 34mm.
embryo (Figure 23, plate II) with that of the 20mm. specimen (Figure 18, plate II) shows
clearly that both differentiation and growth have taken place. The head has rounded out
and is almost protuberant, the mouth is almost closed and looks like a mouth. The gill-
slits have lost the embryonic look even though short filaments are present. The paired
fins show progress. The pectoral-fin base has some of the radial cartilages faintly shown.
The pelvic fin is well differentiated. Even more differentiation is seen in the tail parts.
Noticeable is the development of the dorsal and anal fins and of the dorsal and ventral
lobes of the caudal (the latter lobe being better developed). This caudal, however, has
an even more marked downward swing than that of the 20mm. embryo. The original
drawing of this figure measured 223 mm.
Comparison of this 34-mm. frilled shark in lateral aspect (Figure 23, plate II) with
Scammon’s 34mm. dogfish in like aspect (his Fig. 31, pl. IV) shows that the dogfish is
further advanced in development than the frilled shark. The fins (both median and paired)
of Squalus are much better developed, and from its spiracles and gill-arches extend a great
profusion of long external gills. Its lateral-line system is more prominent. The mouth of
Chlamydoselachus, however, is far better developed than that of Squalus.
AN Emaryo oF 39 MILLIMETERS
Of this specimen, Dean’s “List” calls for drawings, “Entire in three positions”.
This is the first embryo of which there are three full-length portraits.. There are four
other embryos each drawn full length in three aspects—dorsal, lateral, and ventral. For
all five embryos, these full-length drawings will be studied in the order just noted, and the
embryo in each aspect will be compared with the next younger embryo in the like aspect.
Studied in such order one will get the most comprehensive view possible of each stage.
Dorsal Aspect.—The original drawing of this embryo measures 258 mm. and the
magnification is 6.6. As seen in Figure 26, plate IJ, this is a trim-built embryo. The
head is much rounder in front than that of the 34-mm. embryo shown in Figure 22, plate
II, but it is still wide between the eyes. Forward of the first gill-flaps, are found the large
spiracular clefts. The gill-folds are all well developed—the first markedly so. The
pectoral fins are still in about the same stage of development as was found in the 34mm.
specimen. The pelvics, however, show up plainly alongside the slender body. The
dorsal fin and the upper lobe of the caudal are faintly outlined .
Lateral Aspect.—In making this drawing of the 39mm. embryo (Figure 25, plate
IJ), the artist availed himself of artistic license to the amount of 10 mm. over the preceding
figure—the original drawing measuring 268 mm. This specimen will now be compared
with the 34-mm. fish in similar aspect (Figure 23, plate II). In the drawing it is seen that
the head in front of the eyes has elongated somewhat. The olfactory organ has moved
forward with reference to the eye—-which no longer shows the choroid fissure. The
602 Bashford Dean Memorial Volume
upper jaw has elongated beyond the vertical of the eye. The spiracle also has moved
forward and slightly upward, and is now in the vertical of the angle of the jaw. The
gill-straps are still angulate backward at their dorsal and ventral extremities. The first
has the free edge irregular, as though it had been bitten. External filaments are found
in gillopenings 1-4, but are still lacking in the spiracle. The pectoral and pelvic fins
show little progress. The dorsal and anal fins, however, have grown larger. Contrary to
what was found in the 34-mm. embryo (Figure 23, plate II) the caudal fin is bent upward
but the soft parts of the fin seem little larger than they were in the 34-mm. fishlet.
Ventral View.—The original drawing of the 39-mm. embryo in this aspect is also
268 mm. long. This portrayal (Figure 27, plate III) is very instructive when compared
with that of the head only of the 34-mm. fish in like aspect (Figure 24, plate II). The fore-
head is decidedly round. The edges of the olfactory pits are thickened, as if the valves
are beginning to form. The eyes in this aspect are still prominent. The mouth is stretch-
ing forward toward the snout. The lower jaw has taken on something of the form found
in the adult, and the upper jaw no longer has a fossa in the symphyseal region. The an-
terior part of the isthmus is broader in this embryo than in the 34-mm. embryo. The gill-
arches all bear external filaments, those of the first slit being especially long—longer than
they are shown in the lateral view (Figure 25), and longer than they are in the stages im-
mediately following. The hindmost right gill-strap is curiously twisted. The stumpy
pectoral fins show no progress, but the pelvics are well developed and the cloacal eminence
appears between their hinder ends. Faintly outlined in the drawing is the ventral lobe
of the caudal fin..
Brief comparison of the 39‘mm. Chlamydoselachus may be made with Scammon’s
37-mm. Squalus. In the latter, the fins are better developed. On the head the nasal pits
are much more developed, and the latero-sensory canal system shows plainly. If present
on Chlamydoselachus is it not shown in the drawings. The mouth of the frilled shark,
however, is better developed. The embryonic gillfilaments of Squalus are profuse and
long, some still coming from the spiracles. In Chlamydoselachus they are present in the
gill-slits only, but are short and inconspicuous.
The figures of the 37mm. Squalus are the last of Scammon’s drawings made of
specimens. in the flesh. His other figures (text-figures) are reconstructions of serial
sections of these embryos (portrayed in his plates I-IV). Comparisons with the drawings
in his plates have been very instructive and helpful, and it is regretted that his series of
plate drawings does not extend to older and larger embryos.
Tue 39-mM. Emsryo AND ITs YOLK Sac IN Cotor
Colored drawings were made of but three of Dean’s Chlamydoselachus specimens—all
shown on Plate V. Fortunately one of these is of the identical egg of which detailed
figures have just been studied. This embryo and its yolk sac are beautifully portrayed
in Figure 50, plate V. The embryo measures 39 mm. in length and the yolk sac 95 x 65
mm. The yolk stalk averages about 2.5 mm. in width and is about 7 mm. long. This long
The Embryology of Chlamydoselachus 603
and slender yolk stalk allows the embryo considerable freedom of motion. Embryo and
egg are undoubtedly drawn in natural size. No mention of this figure is to be found in
Dean’s notebook.
Proceding out from under the head of the embryo is the single vitelline artery, which,
after traversing about 90° of the circumference of the yolk sac, divides into two. Coming
in under the tail of the embryo is the vitelline vein which receives at right angles many
tributaries. These are abundant in the proximal portion of the vein even to the point
where it enters the yolk stalk. The complete circulatory pattern will be considered
later when older stages are described. Note should be made of the pale pink color of the
surface of the yolk mass. This drawing confirms Nishikawa’s statement that ““The yolk is
of a pinkish color”.
NisHikawa’s 43-mM. Empryo ON ITs YOLK-SAC.
There is no specimen of this size called for in Dean’s list, but such an embryo is shown
in his Figure 7, plate I. Here is the history of this egg as I have reconstructed it.
The egg with the 43-mm. embryo on it which Nishikawa figured in an outline pen
and ink drawing (my Text-figure 4) was redrawn for Dean in pencil for lithographic
reproduction, as may be seen by comparing the outline text-figure with Figure 7, plate I.
This, I conjecture, was done not so much to fill in a gap in the series (there are no large
drawings showing details of the morphology of this embryo) as to show the egg capsule
and the yolk-sac circulation. Here it may merely be noted that the large unbranched
vessel on the yolk is an artery, the much-branched one a vein. This specimen has already
been studied for the structure of the capsule in the section on “The Encapsuled Egg”.
The yolk-sac circulation will be described later. Both original figures—text and plate—
show egg and embryo in natural size. Even in figure 4 (reproduced natural size), the little
fish is too small to show any details.
Dean's Emsryo OF 46 MILLIMETERS
The “List”’ does not call for a specimen or figures of an embryo of this size, but I find
carefully executed drawings in dorsal, ventral and lateral views. Moreover, two of
these drawings are labelled in Dean’s writing. Grouped with the three drawings, of the
46mm. embryo are three each for embryos of 54, 66, and 103 mm. These drawings, all
done in one technique by the same hand and mounted on a different kind of board, look to
me to have been made more recently than any drawings thus far studied and more recently
than single drawings of larger and older specimens to be studied later. All the older
drawings of embryos both smaller and larger than these four are mounted on a poor
quality of yellow cardboard, old, dog-eared, soft and crumbling. The drawings themselves
are yellow with age and often spotted and dirty. These drawings are years older than the
four sets referred to. The most tangible evidence of the technique of the newer drawings
is found in the ““window”’ in the eyes of the figures of these four sets of embryos. There is
no evidence as to where and when they were made.
Dorsal Aspect.—The original drawing of this 46mm. embryo seen from above
measures 257 mm. (i.e, x 5.6). It is reproduced in Figure 28, plate HJ. When this drawing
604 Bashford Dean Memorial Volume
of this embryo is compared with that of the 39-mm. specimen in the same view, it is
seen that the larger embryo has a rounder and shorter snout with eyes somewhat
less prominent and more normal. There are faint traces of the sensory canal system on
the head. The spiracles are smaller, and are more dorsally situated—higher on the
head. The gill-flaps are more widely distended than those of the smaller specimen. The
external gill filaments, lacking in this view in the 39-mm. embryo, are very noticeable
especially in the first, second and third slits, and a few short ones are even found projecting
from the spiracles. Both paired and median fins are better differentiated than in the 39-
mm. embryo, and the artist has been able to portray in outline the dorsal fin and the soft
dorsal part of the tail fin.
Lateral View.—Comparison and contrast will now be made of the 46- and 39-mm.
embryos as seen in side view in Figure 29, plate III, and Figure 25, plate I]. Where the
39-mm. fish is almost straight from head to dorsal fin, the 46-mm. fish has a depression in
the vertical of the spiracle and angle of the mouth. Back of this the little fish is very
sway-backed clear to the dorsal fin. The head of the 46-mm. specimen is shorter and more
flatly rounded. The depth of the head is noticeably less than that of the 39-mm. fish.
The nasal aperture is greatly reduced. Eye and mouth are both closer to the end of the
snout, and the eye is very large. The spiracle is now a narrow slit seemingly not placed so
high as it is shown in the dorsal view of this 46mm. embryo. The first gill-cover seems
either distorted or anomalous, unduly exposing the filaments of the first demibranch. The
39-mm. embryo has only short gill flaments but in the 46-mm. specimen all the slits, but
especially the first, have a profusion of slender external filaments—there are two projecting
even from the spiracle. The paired fins are better developed than those of the younger
specimen. Likewise dorsal and anal fins show much growth. Note that they look cut
off squarely behind. The caudal fin is sharply bent down but the soft parts are devel-
oping well.
Ventral Aspect.—Seen from below (Figure 30, plate II), the 46-mm. embryo is very
much like the 39-mm. one (Figure 27, plate III). The head is narrower and more rounded.
This brings the nasal capsules and eyes closer to each other. The mouth has elongated
somewhat. There is a remnant of a fossa in the median part of the upper jaw. This jaw is
more heavily built and more sharply outlined than that of the younger fish. The mouth
is still widely open and the lower jaw noticeably approaches the form of that of the
adult. The gillarches are widely distended and bear a profusion of external filaments.
The isthmus is very narrow and the first pair of gill-covers is confluent over it. Thus
first of all this embryo of 46-mm. justifies the name assigned this shark—Chlamydoselachus,
the cloak-gilled shark. Lastly, the paired fins are much more developed than those of the
39-mm. specimen, and the cloaca shows conspicuously between the tips of the pelvics.
The artist has also been able to show the anal fin and the lower lobe of the caudal.
The head of this 46mm. embryo in both dorsal (Figure 28, plate III) and ventral
(Figure 30, plate III) aspects seems entirely normal. But portrayal from the side shows
a head which seems abnormal in every respect (Figure 29, plate III). One almost doubts
if the three drawings were made from the same embryo.
The Embryology of Chlamydoselachus 605
Heap or A 48-MM. SPECIMEN IN VENTRAL VIEW
We now return to Dean’s “List’’, which calls for ““Embr. of 48 mm. ventral (head)””
and on the opposite page is “48? Another, head only stained’. Among the older draw-
ings I find one without the figures “48” but with the significant label “head only stained”.
Moreover the drawing (Figure 31, plate II) shows this head in ventral view. From these
data, and despite the fact that this “head . . . stained” in ventral view looks somewhat
younger than the head of the 46mm. embryo in ventral aspect and decidedly younger
than that of the 54-mm. specimen (Figure 34, plate III), I believe that this head shown in
ventral view is that of the 48mm. embryo. Nishikawa had a 49-mm. specimen, and |
believe that the “head only, stained” shown in Figure 31, plate II, is Nishikawa’s speci-
men stained in toto (as was the practice in those days) but never sectioned.
Compared with the 46mm. embryo (Figure 30, plate III), the head looks wider and
more rounded, the eyes less prominent and the nasal organs better developed. The mouth
is less advanced than that of the 46mm. specimen. The upper jaw still has a definite
median gap between the two halves, but the lower seems to be about normal for this
stage. The gill-flaps are widely spread, especially the first pair—which are not continu-
ous across the isthmus. Filaments seem to be absent, save in the first and second gill-slits
on the right side. The pectoral fins are hardly so well developed as those in the 46mm.
embryo. The gular fold is lacking. That the 48mm. embryo seems younger than the
46mm. specimen is probably an individual variation.
Nisoikawa’s 50-mM. Empryo on 17s YOLK Sac
Nishikawa (1898) had a 50mm. embryo of Chlamydoselachus on its yolk sac. He
did not have either yolk sac or embryo drawn, but he does portray the head only in both
dorsal and ventral aspects (Text-figure 28a and B). Whether Dean got a specimen of
this size, through the help of Kuma or the commercial fishermen, cannot be said. But
I suspect that Dean’s drawings of egg and embryo (Figures 9 and 10, plate I) were made
from Nishikawa’s specimen. I have shown that Dean’s Figures 7 and 8, plate I, are
duplicates of Nishikawa’s Figs. 1 and 2 of his pl. I. Here compare my Text-figure 4 with
Figure 7, plate I. Now the capsules of the egg seen in Figures 7 and 9 plate I, are of the
same type. Dean may have had eggs with capsules such as these, but, since no others of
this kind are figured by him, I doubt it. In my judgment, the egg with the 50mm embryo
is the one listed by Nishikawa, and, since it had not been drawn for Nishikawa’s article
(1898), it was turned over with other specimens for Dean’s studies.
On its Yolk Sac.—This 50mm. embryo (shown in half size in Figure 9, plate I) is
of course too small (even in Dean’s drawing in natural size) to show any morphological
details. It was probably drawn to show the capsule and the circulation over the yolk sac.
The capsule has already been studied. It is a counterpart of that around the 43-mm.
embryo and its yolk sac. The yolk circulation is somewhat more advanced than that on
the yolk of the younger specimen. It will be discussed shortly. Fortunately the details
lacking in Figure 9, plate I, may be found in Nishikawa’s line drawings of the head (his
Figs. 7 and 8, plate IV) which will now be considered.
606 Bashford Dean Memorial Volume
A Aorta i |
Text-figure 28
Head of a 50mm. Chlamydoselachus anguineus in two aspects; A in left-oblique
dorsal view, B as seen from below.
After Nishikawa, 1898, Figs. 7 and 8, pl. IV.
Head Only, Dorsal View.—Nishikawa’s drawing (my Text-figure 284) was made in
oblique-dorsal view. In it the front head is bluntly rounded. Being drawn in large
scale, it shows the sensory-canal system on the head with the lateral line extending
backward onto the body. The small spiracular cleft is devoid of filaments. The gill-covers
are distended (the first very widely) and abound in external gill-filaments—some of which
appear to be longer than any thus far noted. It is difficult to compare this head with
that shown in Figure 28, plate HI.
Head Only, Ventral Aspect.—The 50mm. head (Text-figure 285) must be com-
pared with that of the 48mm. in the same view. The heads seem (as might be expected)
to be in practically the same stage of development. The 50-mm. head is slightly more
pointed. Eyes and nostrils show no perceptible divergence in the two specimens.
Mouths are alike save that the upper jaw of this specimen has no fossa in the symphyseal
region. The gillarches are shown widely distended and, unlike those of the 48mm.
head, are filled with protruding filaments—those on the left side being the more abundant
and certainly the longer. They are found on both sides of the five hinder arches. The
gular fold is barely continuous across the isthmus.
The Embryology of Chlamydoselachus 607
An Empryo or 54 MILLIMETERS
In Dean’s “List”’, the next call is for “Embryo of mm.55. Entire—draw dorsal and
ventral views [of head]”. These drawings I find. But, in the plates of newer drawings of
later origin (as noted above), I find three fulllength drawings—in dorsal, lateral and
ventral aspects—of an embryo labelled “54 mm.” in Dean’s writing. The full-length
figures of the 54-mm. specimen will now be contrasted with those of the 46mm. embryo.
The figures of the 55mm. fish (belonging to the older set of drawings) will be studied
next. Each of the original drawings of the 54mm. embryo measures 257 mm.—i.e.
is multiplied by 4.7.
Dorsal Aspect.—When comparison of this drawing (Figure 32, plate III) is made
with a similar one (Figure 28, plate III) of the 46-mm. specimen, the head and trunk are
found to be notably larger. The fish is decidedly like an elongate tadpole. The latero-
sensory canal system on the head is clearly seen. The first gill-covers are not so widely
spread. From all the gillslits profuse elongate filaments contrast with the shorter
ones of the younger embryo. Then, too, from the spiracle protrude more and longer
filaments. The pectoral and pelvic fins show decided growth, but in this aspect one
cannot say about the dorsal fin and the upper lobe of the caudal. The body between
pectorals and pelvics is relatively shorter than in the 46-mm. embryo.
Lateral View.—Marked contrasts may be drawn between the 54- and the 46-mm.
embryos seen in lateral aspect (Figure 33, plate III, and Figure 29 on the same plate III).
The 46mm. fish is very sway-backed, the 54mm specimen has a marked concavity in
the neck region but behind this it is moderately hump-backed and has something of the
look of the adult fish. The head is rounder and better developed than in any previous
stage. The pits of the latero-sensory canal system are well developed over head and
first gillcover. The lower jaw has become greatly elongated and faintly recalls that
of the adult. The almost vertical hinder edge of the first gillcover contrasts marked-
ly with the open U-shaped structure of the 46mm. specimen—which is probably
anomalous. The external gillfilaments are well developed. Some are found in the
spiracle, which is much higher up on the side of the head than that of the 46mm. fish.
Both paired and unpaired fins of the 54-mm. fish are somewhat better developed than
those in the younger one. The tail of the present fishlet is as much bent up as that of the
46mm. specimen is bent down. Other than this, the tail regions are much alike.
Ventral Aspect.—Considerable contrast is to be noted when the two fish are com-
pared in ventral view (the 54-mm. in Figure 34, plate III, and the 46mm. fish in Figure
30 of the same plate. The head of the 54-mm. specimen is much broader as was noted in
dorsal aspect. The eyes are larger, the openings of the olfactory slits smaller. The pits
of the latero-sensory canal system show clearly. The mouth shows marked develop-
ment—it resembles that of the adult but is still ventral in position. The first gill-covers
form a wide cloak covering the isthmus. The gillarches—standing out fairly at right
angles in the younger specimen—are here bent somewhat backward. Every gill-slit is
crowded with external filaments which reach their maximum development here. Trunk
608 Bashford Dean Memorial Volume
and paired fins show some development, and anal fin and lower lobe of caudal are shown
in wavy outline. As one would expect by referring to Figure 33, plate III (the lateral
view), the dorsal and anal fins and lobes of the caudal are practically continuous. Along
the mid-ventral line is a ridge which I take to be the beginning of the tropeic folds. Note
how much like a tadpole the little fish appears.
Aw Empryo Measurinc 55 MIimeters
As noted above, Dean’s “List” calls for drawings of the entire embryo and dorsal and
ventral views (presumably of the head) of an embryo of this size. These three drawings
I find, but, since they look old and are mounted on discolored cardboard, I conjecture that
they were made in Japan in 1901-02. They will be compared with the later-made draw-
ings of the 54mm. specimen. The full-length drawing of the 55-mm. embryo in lateral
aspect measures 238 mm. (= X 4.3+).
Head Only, Dorsal View.—It is now in order to contrast the head (Figure 35,
plate III) of the 55mm. embryo with the head of the 54mm. specimen shown in full
view in Figure 32, plate II]. The 55-mm. head seems narrower but is rounded like the
other, the eyes are a little further forward, and the sensory-canal system shows very
indistinctly. The spiracles seem larger but show no gill filaments. Nor are any filaments
visible in the widely separated gillarches. One queries why the 54mm. embryo has and
the 55-mm. one lacks these external flaments. Note that the pectoral fins of the 54mm.
fish have little hook-like spaces between fin and body, while these are lacking in the older
embryo. In general it can be said that, contrasting the heads of two specimens, one gets
the impression that the 55-mm. head looks more finished—i.e., older.
Full-length, Lateral Aspect.—The fulllength lateral-view drawing of the 55-mm.
specimen (Figure 36, plate III) will be contrasted with the like drawing (Figure 33, plate
III) of the embryo of 54mm. Naturally the differences between them are individual
rather than of stages of development. The original drawing of the 55-mm. fish measures
238 mm. (i.e., X 4.3+), that of the 54mm. one measures 257 mm. (1.e., X 4.7+). In the
55-mm. embryo, head and trunk are straight above and the head rounds off forwardly to
a rather distinct snout. The nasal apertures are situated well forward almost in their
definitive position. The lower jaw is not so long as that of the 54-mm. embryo. The
lateral-line system shows plainly on the trunk but on the head is hardly so well-developed.
The gill-covers (especially the first) are also hardly so well developed and the external
filaments are not nearly so long as those in the 54mm. fish. The spiracle of the 55-mm.
specimen is higher on the head and contains several short gillfilaments. Of the fins,
pectorals, pelvics and dorsal are about equally developed in both embryos. The anal fin is
better developed and more sharply marked off from the lower lobe of the caudal in the
55-mm. embryo. The caudal fin droops, whereas that of the 54-mm. fish swings upward.
Unfortunately the artist has used dark lines to indicate some grooves between somites,
which thus appear like branches of the lateral-line canal.
Head Only, Ventral View.—Perhaps most instructive will be a comparison of the
under surfaces of the two heads—the 55-mm. specimen in Figure 37, plate III, and
The Embryology of Chlamydoselachus 609
the 54mm. in Figure 34, plate HI. The head of the former looks decidedly older than
that of the latter. The head in front of the mouth is shorter, and across the mouth
region it is narrower. The nasal cavities are located well forward. The mouth of the
55-mm. fish looks less embryonic, older and better developed. The gill-arches are not so
dilated and the filaments are, as noted above, entirely lacking. In both, the first gill flap
is continuous across the isthmus. The sensory-canal system on the under side of the
head is well developed.
Here are two embryos differing in length by but one millimeter, but varying widely
from each other. The morphological differences are principally in the head and mostly in
the ventral head. In degree of development the mouth structures so differ that, on the
basis of this one character with no others visible, one would separate these embryos as of
two widely different stages. Whether this represents an actual difference in embryos
of a shark whose variableness is greater than in any other known to me, or is due to a
difference in artists cannot be said. Were the two embryos at hand, the matter might
possibly be settled.
GarMan’s Empryo or 64 MILLIMETERS
When Dr. Thomas Barbour, now Director of the Museum of Comparative Zoology,
Cambridge, Mass., returned in 1906 from a visit to Japan, he brought with him this
embryo. It was figured but not described by Samuel Garman in 1913 (Figs. 7 and 8,
pl. 61). For its historical interest and for the sake of completeness, Garman’s figures
(lateral and ventral aspects) are reproduced herein as text-figures and are described.
Lateral Aspect.—Comparison must be made of the 64-mm. embryo (Text-figure
29a) with that of 55 mm. (Figure 36, plate III). Excepting in the head region, the two
Text-figure 29
Two views (lateral and ventral) of a 64-mm. embryo of Chlamydoselachus.
After Garman, 1913, Figs. 7 and 8, pl. 61.
610 Bashford Dean Memorial Volume
drawings show embryos much alike. The head of Garman’s fish is thinner and is smoothly
rounded down to the upper jaw. Dean’s specimen is thick in head and gillregion and the
head rounds steeply to the upper jaw. The mouth of the 64mm. embryo is in about
the same stage of development as that of the 55-mm. fish. The spiracle of Garman’s
fishlet is not so high on the head as that of the other embryo but is elongate vertically
and has more gill filaments protruding. There is some slight difference in the shape of the
gill-openings, but both little fish are well supplied with external filaments. Remarkably
alike are the fins, paired and unpaired. Both tails have about the same droop.
In Ventral View.—Garman’s full-length figure of his 64-mm. embryo in this aspect
is shown in Textfigure 298. For adequate comparison we must turn to Figure 37,
plate III, Dean’s 55-mm. specimen in ventral head aspect. Garman’s embryo has the
mouth not quite so well developed, and the nostrils are not placed so far forward. The
first gill-cover in each fish is continuous across the isthmus. Garman’s specimen (Text-
figure 29s) has a great number of short filaments protruding from each slit. Dean’s fish
has none showing in the figure in ventral aspect (Figure 37, plate III) although they are
portrayed in the lateral view (Figure 36 on the same plate). As Text-figure 29s shows,
the 64mm. embryo has the pelvic fins well developed. Note the cloaca between their
hinder ends. Anal and caudal show in the drawing. The pectoral fins and the yolk
stalks look much alike.
These drawings (Text-figures 29a and B), made ona much smaller scale than Dean’s,
show few details. The specimen, loaned by Dr. Barbour, is before me as I write, and I can
testify that the little fish is accurately drawn. The inclusion of Garman’s figures herein
help make the transition between the 54mm. embryo and that now to be described.
Dean's Empryo Measurinc 66 MILLIMETERS
Third in the series of drawings of embryos noted above as being done by a different
hand and at a later time, is the embryo under consideration. In the original drawings
this 66mm. sharklet is enlarged to 256 mm. (i.e., is x c 3.9). Seeking a younger embryo
with which to compare it, I have made only secondary comparisons with Garman’s
64mm. specimen as being too close and because his figures show too few details. I have
also passed over Dean’s 55-mm. embryo which has but one full-length figure. Direct com-
parison will be made with the close neighbor of the 55mm. embryo, the more typical
54mm. fishlet, which like the present specimen, is portrayed in all three aspects.
Dorsal View.—Comparison of this 66mm. embryo with the 54mm. specimen—the
former in Figure 38, plate IV; the latter in Figure 32,pla te III—shows that the 66mm. fish
is plainly older. The front curve of the head is flatter, the eyes are prominent, the con-
striction back of the eyes is greater, but the sensory-pore system is hardly so clear. The
gillcovers are widely distended, and there is still a profusion of external gill flaments—
but these are shorter and those in the spiracle are fewer. The differentiation in the trunk
region, faintly foreshadowed in the dorsum of the 54mm. fish, is here far more clearly
The Embryology of Chlamydoselachus 611
marked. This is to be seen all the way from head to the dorsal fin. Pectoral and (especial
ly) pelvic fins show development. The dorsal fin is now clearly seen in the drawing and
the upper lobe of the caudal stands out on the thicker vertebral part of the tail.
Seen from the Side.—More marked are the differences in the lateral views of the two
embryos—the older (66 mm.) shown in Figure 39, plate IV, and the younger (54 mm.) in
Figure 33 on plate III. The head of the older specimen is smaller and is curiously round-
ed. The eye is larger, the nasal groove has moved forward. The mouth is closed and the
lower jaw is plainly longer. The spiracle is placed in about the mid-lateral line whereas it
is above it in the 54-mm. fish. The first gill cover has a ragged or frilled edge and seems
retracted—as it is in the 54mm. fish and (particularly) in the 46mm. specimen (Figure
29, plate III). The gill-filaments in general are smaller, fewer and not so far protruded.
The ‘‘back-of-the-neck”’ hollow seen in Fig. 33 has here become a great “sway-back”” de-
pression, giving the idea of a definite neck between head and body. The body is more
humped than that of the 54mm. embryo. The paired fins show growth. Dorsal and
anal are larger and better differentiated. The tail bends gracefully downward. The
ventral lobe is here sharply separated from the well-developed anal fin, unlike the close
approximation seen in the 54mm. fish. This is the earliest embryo showing the tail fin
in approximately the adult condition.
Dean’s 66-mm. embryo contrasts strongly with Garman’s 64mm. specimen. It has
the top of head high and rounded. In the neck region it has a long “sway-back”, the body
is decidedly arched, and the tail behind the dorsal-anal vertical bends down strongly.
The dorsal region of Garman’s fish (Text-figure 29a) is nearly straight, having at most
very flat curves. Even more difference is to be found in the shape of the gill-flaps. Those
of Dean’s fish are convex posteriorly, save the first which has a frilled edge standing nearly
vertical. For the rest—mouths, spiracles, fins, and tail-tips are very like each other.
In Ventral Aspect.—Seen from below (Figure 40, plate IV), the 66mm. fish
shows considerable development compared with the 54mm. specimen (Figure 34, plate
III). The head in front of the mouth is greatly shortened and more blunt. This has
brought nares and eyes closer to the front of the head. The long mouth begins plainly to
foreshadow that of the adult. The inner surface of the upper jaw is serrate, probably due
to the presence of rudimentary teeth which have not yet erupted. Both upper and lower
jaws are narrower in the transverse and longer in the sagittal plane—more like the adult.
The head, back of the angle of the jaws, shows a marked constriction. The sensory-
canal system is clearly portrayed. The gill-covers are still pretty widely distended, but
with their outer edges bent toward the rear. The gill-filaments still protrude but less than
in the preceding stage. The confluent first gill-covers form a convex U over the isthmus.
Pectoral fins show little difference from those of the 54-mm. fish, but the pelvics are much
further developed. The cloaca has become a longitudinal slit and on either side of its
hinder end the abdominal pores make their first appearance. As in the 54mm. embryo, so
here, in the mid-ventral line is the rudiment of the tropeic folds. The anal fin and the
ventral lobe of the caudal are fairly distinct.
612 Bashford Dean Memorial Volume
When Figure 40, plate IV (the 66-mm. embryo) is compared with Text-figure 20
(Garman’s 64-mm. specimen), it is plainly seen that the two embryos are very much like
each other. The heads are alike broad and blunt. The distance from the center of the
upper jaw to the tip of the snout in the 66mm. specimen is shorter than in the other.
The first gill-covers in each are confluent across the isthmus—with a blunt backward
central point in Figure 40, plate IV, and a straight line across in Text-figure 298. Both
heads in this aspect show a profusion of external gill-filaments in each gillopening. In
the 66mm. embryo, there is seen the beginning of the tropeic folds reaching from yolk
stalk to cloaca. Nothing of the sort is to be seen in the 64-mm. fish.
AN Empryo 103 MM. IN LENGTH
This embryo, the last of the new lot of four drawn in three aspects, is about one and
one-half times the length of the 66mm. fishlet, but in the original drawing it measures
approximately the same—257 mm. (i.e., x 3.9).
Seen from Above.—The merest glance shows that this 103-mm. fishlet (Figure 41,
plate IV) has advanced much over the preceding stage (Figure 38, plate 1V). The head is
smaller, more compact, more finished looking. The latero-sensory canals are well develop-
ed. The spiracles are so reduced in size that the external openings are barely visible. The
gill-covers are far less distended than in the 66-mm. fish, and the filaments are somewhat
fewer but generally longer. The paired fins show marked growth and the dorsal is some-
what in evidence.
In Lateral Aspect.—Seen in side view (Figure 42, plate IV) and in contrast with the
like aspect of the 66-mm. specimen, it is apparent that the larger embryo has gone forward
markedly in development. It now begins to look like the adult. Note the pointed snout
and the long mouth with the fold above, marking off the jaw cartilage. Eye and nasal
opening are in their normal positions. All the gill-covers are for the first time distinctly
frilled. The external gillfilaments are still persistent. The lateral-line and head-canal
systems are continuous. The fins, paired and unpaired, are well developed. The tail is
straight and the lower lobe of the caudal has a faint notch near the tip. The little shark
begins to look snake-like—anguineus.
Seen from Below.—In this aspect the 103-mm. fish (Figure 43, plate 1V) looks more
developed than does the 66-mm. embryo (Figure 40, plate IV). The head is narrower and
more pointed. The mouth is slightly narrower and the lower jaw considerably longer—1t
distinctly recalls that of the adult. The gill-covers (especially the first pair) are seen to
be frilled. They are less distended than those on the heads previously studied. The
external gill-filaments persist and protrude. Both the paired fins, the pectorals especially,
show much development. The cloacal opening looks as though it might be functional,
and the abdominal pores are prominent. On the midline of the ventral trunk is the
tropeic ridge and on either side the somites show distinctly.
An Emsryo or 124 MILLIMETERS
Having finished the study of the later-portrayed series of embryos shown each in
three full-length drawings, we will now proceed to a consideration of some figures of
The Embryology of Chlamydoselachus 613
older embryos drawn at an earlier date and recorded in Dean’s notebook. Here the
“List” reads for the next stage—“Embr. of mm. 123 entire. Ventral (head) dorsal head”’.
I do not find such figures, but I do find a full-length lateral drawing and another of a dorsal
head, both marked “124”. These drawings I take to have been made from the specimen
referred to—the difference of one mm. being insignificant. Whether or not the “ventral
head” was drawn cannot be said. But on the plates as made up by Dean, I find occasional
scars on the board where drawings have been removed. It is of course possible that the
drawing of the “‘ventral head” of this stage has been removed and lost. The drawings of
the 124mm. embryo will now be studied in comparison with those of the 103-mm.
specimen—the preceeding stage.
Head in Dorsal Aspect.—When comparison is made of the drawing (Figure 44,
plate IV) of the “dorsal head” of the 124-:mm. embryo, with that of the head of the 103-
mm. fish (Figure 41, plate IV), it looks older, more finished. The head of the 124mm.
fish looks longer and narrower, and the eyes are less conspicuous. The spiracle is not
visible, being probably too small to show in this low magnification (x 2+, the same
magnification as Figure 45, plate IV, the fish in lateral view). The gill-covers are some-
what distended but reveal no trace of gillfilaments. The lateral-line system shows on the
trunk but is indistinct on the head. The pectorals are smaller. One wishes for the draw-
ing of the “ventral head” to show the form of the mouth and the ventral parts of the gill
covers, especially the first.
Full-length Lateral View.—It was noted that the 103-mm. fish, portrayed in lateral
view in Figure 42, plate IV, showed some decided resemblance to the adult form. How
much more is this true of the 124-mm. specimen seen in Figure 45, plate IV. Here the
whole fish is plainly a young Chlamydoselachus. Note the pointed snout, the forwardly-
placed nasal aperture, the eye in about the vertical of the middle of the mouth, the long
lower jaw reaching close to the end of the snout. The gill-covers (the first much the
larger) decrease in length normally from Ist to 6th, and have their dorsal edges backwardly
bent as in the adult. No gill- filaments can be seen. The spiracle is not shown in this
drawing, even though the original measures 257 mm. in length—t.e.,x 2+. The pectoral
fin is much larger than that of the 103-mm. specimen, but the pelvic is of about the same
size. The dorsal and anal are somewhat smaller than these fins are in the younger fish.
The back is nearly straight from head to dorsal fin. The body has elongated, not in the
tail region but in the body proper, i.e., between pectoral and pelvic fins. The tail ends in
a fine-pointed caudal fin which droops slightly downward. The soft parts of the caudal
fin are smaller than those of the 103-mm. fish. The lateral line is well developed and
shows an interesting curvature behind the vertical through the tips of caudal and anal.
An Empsryo or 175 MM. AND ITS YOLK SAC
The “List” next calls for “Embr. of mm. 175, entire, dorsal aspect with yolk”. This
I find as portrayed in Figure 11, plate I. In the original drawing, the fish, measured
carefully over the curves, is 205-mm. long and the yolk sac measures 92 x 90 mm. On the
page of Dean’s notebook opposite the ““List”’ is a record of seven specimens taken “April
614 Bashford Dean Memorial Volume
=f
25°. Among them is a specimen of 205 mm. This I judged to be the specimen drawn
and I concluded that it was drawn in natural size since the embryo of Figure 11, plate I
measures 205 mm. around the curves. Furthermore, it seemed that a yolk sac 92 x 90 mm.
would not be too large for an embryo of this size. But the figure bears in Dean’s writing
the notation “175” and the last embryo of the seven taken “April 25” is listed as “175”
mm. So it seems clear that, in the original drawing, the 175mm. embryo and yolk sac
are enlarged 1.2 times. There is no drawing of the 205-mm. embryo.
Seen from Above.—The only embryo with which to compare this 175-mm. specimen
(Figure II, plate I) is that of 124-mm. and of it the drawing of the head only (Figure 44,
plate IV). The head of the 175mm. fish looks distinctly older even though the remnants
of external gill filaments show in the arches. In contrast, the snout of the little 175-mm.
fish is blunter than that of the 124mm. embryo, the eyes far less prominent, and the gill
covers far less spread out. The presence of gill filaments even though small, is not un-
usual since they are found in far older specimens as will be seen later. The pectoral and
pelvic fins have a decidedly “grown up” appearance. Dorsal and anal fins are well de-
veloped and the lower lobe of the caudal looks very much like that of an adult. The tip
of the caudal is bent downward and is devoid of a notch. The lateral-line system is
clearly marked, and the latero-sensory canals and ampullae on the head are well delineated.
On the trunk region, the lateral line grooves appear to be connected across the dorsum
by transverse broken lines drawn in white. These are like those shown in the tail-region
of the 55mm. embryo (Figure 36, plate III). They are surely inter-somitic grooves, not
portions of the lateralline system. This portrayal (Figure 11, plate I) shows the vitelline
circulation in an advanced stage of development. It will be considered shortly. Alto-
gether this is the most artistic drawing thus far found.
Aw Emspryo 185 sar. iy Lencta
Dean’s “List” calls next for an embryo of 185 mm. to be drawn full-length in lateral
aspect without yolk. This drawing is reproduced herein as Figure 46, plate IV. The
original drawing measures 185 mm., hence is natural size—the first of the embryos so
drawn. This little fish looks very like an adult even though it was attached to the yolk
sac by a yolk cord measuring 11 mm. in diameter. To see how far this embryo has
progressed, it must be compared with the 124mm. specimen (Figure 45, plate IV),
seen in the same aspect. (The 175mm. embryo cannot be used in comparison, since it
is portrayed in dorsal aspect, and is moreover not drawn straight). The snout of the
185-mm. fishlet is more pointed (dorso-ventrally compressed); nasal capsule and eye are in
their normal positions. The long lower jaw brings the mouth almost to the terminal
position. The gillflaps are nearly as normal as those of the fine 124mm. embryo, which
lacks the remnants of gill filaments present in the 185-mm. fish. The body is humped
and on it is a well-developed lateral line with latero-sensory branches on the side of the
head, and with marked bends under the dorsal fin. Above the lateral line, the artist has
inserted broken lines as if they were branches of the lateral line. They are spaced to
correspond with the grooves between the myotomes immediately ventral to the lateral
The Embryology of Chlamydoselachus 615
line. The paired fins have well-developed bases. The dorsal and anal fins look much like
those in the adult fish and even more is the caudal like the tail fin of an adult Chlamydo-
selachus. The tropeic folds, noticeable in the 103-mm. fish, are here plainly visible.
Head in Ventral Aspect.—The list calls only for “Embr. 185 mm. lateral aspect”.
It does not call for ventral view of the head, but such a drawing I find. This is reproduced
as Figure 47, plate IV. The next youngest head in like aspect with which it can be
compared is that of the 103-mm. embryo (Figure 43, plate IV). Here one sees that the
profuse external gillfilaments of the 103-mm. head are reduced to mere remnants in
the gillslits of the 185-mm. fish. Furthermore, the mouth of the older fish looks more
finished, more nearly adult. The first gill-flaps are continuous across the isthmus. These
flaps show some evidence of being “‘frilled”. In the 103-mm. embryo, the yolk stalk has
been cut off close to the body. In the 185-mm. fish the basal part is shown attached to
the body. This is very large and I judge that here it is really part of the sac that is seen,
that we have here the attachment of body to yolk directly comparable to that seen in the
390-mm. shark portrayed in color (Figure 49, plate V).
A Youne Frittep Suark 240 mm. Lone
The next embryo on the “List” is one of this size to be drawn in full length, lateral
aspect, without yolk. This little fish was drawn slightly smaller (3 mm.) than natu-
ral size. As Figure 48, plate IV. shows, it is even more like the adult than is the 185-
mm. specimen (Figure 46, plate IV). The long mouth has nearly attained the terminal
position, nostril and eye call for no remarks, the gillflaps are frilled and show short
filaments in the openings. There isa small spiracular opening precisely in its adult location.
All the fins are better developed and even more closely resemble the adult organs than
those of the preceding stage. The lateral line runs the full length of the body and shows
only very slight variations under the dorsal fin in contrast with both the 185- and the
124mm. young. The little fish is still attached to its yolk sac by a cord 7 mm. in diameter.
The caudal, like that of the 185-mm. fish, is slightly bent upward.
A 390-mM. CHLAMYDOSELACHUS IN NATURAL CoLors
Next and last, Dean’s “List” calls for four embryos to be drawn. These were “taken
about May 1, 1905”, and were “Bt. in Tokyo, June 20”. They measured in millimeters
317, 331 (yolk sac, 111 x 100), 352 and 390 (yolk sac, 100 x 90), and probably all came from
one mother. However, since they were presumably twins and since the youngest differed
from the largest embryo by only 38, and the others by 59 and 73 mm. respectively, it was
clearly unnecessary to go to the expense of having all four drawn. So Dean seems to
have compromised by having the largest specimen drawn in color. This exquisite drawing
is accurately reproduced in the original colors as Figure 49, plate V.
It may be of interest to attempt to reconstruct the history of the specimen and of the
drawing. Since the four embryos were “taken about May 1, 1905” and “Bt. in Tokyo,
June 20”, they must have been in preservative about seven weeks before they came into
Dean’s possession. Now Dean states (1901) that he had the active cooperation and
616 Bashford Dean Memorial Volume
effective help of Prof. Mitsukuri of the Imperial University of Tokyo to the end that all
specimens of Chlamydoselachus taken in the Gulf of Tokyo should be reserved for him
(Dean). Hence one may judge that the fish had been taken by the fishermen to the Depart-
ment of Zoology in the University, there opened and the embryos secured for Dean.
The original drawing (Figure 49, plate V) measures 382 mm. between perpendiculars,
and the yolk sac is 92 x70 mm. If the fish was drawn alive or just dead, the discrepancy
of 8 mm. between its length and that of the largest of the four embryos listed above
(390 mm.) may be disregarded, as it may for the discrepancy in yolk measurements (92 x 70
in the figure vs. 100 x 70 mm. in the notes). These may be errors of the artist. But I have
shown earlier in this paper that embryos brought up within the mother from a depth of
300 to 500 fathoms, from a region of great pressure and low temperature, to the University
of Tokyo in May, could only have survived a few minutes. Here then is what I judge to
have been done when this specimen came in. A quick sketch in color was made while
embryo and yolk were fresh. Then to preserve it, the fish was put in formalin (which
bleaches out color less than alcohol). Later, and as soon as possible, the completed draw-
ing was made—the size from the specimen in preservative, the color from the hasty color
sketch. The embryo in preservative for a month would easily have shrunk 8mm. The
shrinkage of 8 mm. in the length of the long axis of the yolk is entirely within the limits
as I have observed it in the large yolks of other fishes. To strengthen this case it may be
noted that among Dean’s frilled-shark materials there is a water-color sketch of the
reproductive organs of a just-opened female Chlamydoselachus evidently intended as
the basis of a figure in natural color. Unfortunately this drawing was never made or has
been lost. But we do have here this beautiful drawing showing this late embryo, the
yolk sac, and on the side of the egg the yolk-sac circulation, all in their natural colors.
There is in the Museum collection—it stands before me as I write—what I believe
to be the very specimen from which the drawing (Figure 49, plate V) was made. The
shape of the head and mouth, the fold across the snout above the upper jaw, the form and
position of the gill-slits, the upturned pectoral fin, the form and position of the other fins
and the tail, the irregularities in the lateral line, the shape and position of the yolk sac—all
are practically identical. This is surely the fish from which the drawing was made. The
fish, after at least 33 years in formalin and alcohol, measures 370 mm. in total length and
the yolk mass 78 x 60 mm. But those who have had to do with specimens in preservative
know that this decrease in the size of the fish is not beyond limits. However, the yolk has
undergone even greater shrinkage than the fish. The ordinary fish-egg yolk shrinks con-
siderably in preservative, but there is in the egg yolk of Chlamydoselachus an additional
factor in its shrinking. There is in these yolks an unusual amount of oil which is dissolved
out by the alcohol. This alcohol, even to this day, has to be changed frequently. This
dissolving of the oil aids materially in the diminution of the volume of yolk as it hardens.
The likeness of this 15.35-inch embryo to an adult is close both in the general mor-
phology and in the details. The mouth, reaching far back of the eye, is almost terminal
and evidently has a great gape. There is the groove marking off the cartilage of the upper
The Embryology of Chlamydoselachus 617
jaw. The nasal aperture of the embryo is not yet completely divided into two. The
gillcovers have pocket-like folds where they join the body. The first plainly extends
across the throat—i.e., the isthmus and throat are “cloaked’’. Note that there are visible
very short gill-filaments. The body is humped above and on the ventral edge is seen one
side of the tropeic folds.’ Plainly visible is the latero-sensory canal on the first gill-cover
and the lower jaw, and the lateral line extending along the body and the tail to its very
tip—with the previously noted irregularities under the dorsal fin.
In this drawing, the artist has again inserted short dotted lines (in white) extending
dorsally from the lateral line. These are more widely spaced than the zigzag intersegment-
al grooves seen along the sides of the body. Examination of the original specimen and of
one but slightly smaller discloses that the intersegmental grooves above the lateral line are
occasionally visible. Nothing in this region in this fish could easily be mistaken for branch-
es of the lateral line.
The fins are very like those of the adult, including the well-formed caudal fin with
the notch at the tip of the lower lobe—faintly presaged in the 103-mm. fish, but here seen
plainly for the first time in this drawing of a large frilled shark embryo. What more can
be said in description of this striking figure? The reader must study it for himself. -
THE YOLK-SAC CIRCULATION
The vitelline blood vessels from small beginnings come finally to spread over all
the large yolk sac of Chlamydoselachus. Their function is to bring food stuff to the de-
veloping embryo. These vessels have been briefly referred to earlier in this paper in
describing certain embryos figured on their yolk sacs—the 39-mm. embryo (in color), the
43- and 50-mm. embryos and the 175-mm. fishlet (in gray), and lastly the 390-mm. shark
(in color). The early stages of the development of this circulation are lacking in these
drawings but the intermediate and later stages are shown. These portrayals are so in-
formative as to call for special study.
Opportunities to study the yolk-sac circulation on the eggs of sharks occur very
infrequently. In my investigations on live eggs and embryos of the sharks and rays else-
where referred to, I was so occupied with other observations that those on the yolk-sac
circulation were very incomplete. Dean’s figures unfortunately do not show the early
stages, so to make things clear, I refer the reader to Balfour’s classical work (1885, pp.
465-466, pl. 9). In this he figures (diagrammatically) and describes the early circulation
on the egg of Pristiurus essentially as it will presently be portrayed for Chlamydoselachus.
Here is a synopsis of what he wrote.
As may be seen in Text-figure 30a, the blastoderm in this early stage covers about
three-fifths of the yolk. The embryo is found in the bay of the blastoderm and from under
its head extends forward the vitelline artery (a). This presently divides into two forks
right and left and these are the beginnings of the arterial ring. In Text-figure 30s, it 1s
For data concerning this extraordinary structure, found in no other shark, the reader must turn to Gudger and Smith (1933,
Article V of this Memorial Volume, pp. 283-284, Text-figure 12) by whom it is figured and comprehensively described.
618 Bashford Dean Memorial Volume
Text-figure 30
Three diagrammatic figures showing the development of the vitelline circulation on the
egg of Pristiurus. A is a beginning, C an intermediate, and D an advanced stage.
a, vitelline artery; v, vitelline vein, yk, yolk blastopore, y, (in C) marks the spot where the venous ring and yolk
blastopore were closed by the growth of the blastoderm.
After Balfour, 1885, Figs. 1, 2, and 3, pl. 9.
seen that the blastoderm has grown over all the yolk save a central area (the so-called yolk
blastopore, yk), forward of which the embryo is found. The two arms of the vitelline
artery (a) are in the act of joining behind to form the arterial ring. These arms give off
many small arteries on the inside of the hinder half of the ring. Surrounding the yolk
blastopore, a venous ring has arisen in the edge of the blastoderm. From its anterior part,
there has developed a main venous trunk which reaches to the yolk stalk. The venous
ring receives many veinlets on its outer side.
In Text-figure 30c, the vitelline circulation has made much progress. The arterial
ring is complete, has increased in size, and even in the anterior region gives off many small
arteries. The yolk blastopore has disappeared, due to the complete enclosure of the yolk
by the growing blastoderm. The letter y marks the point of closure of the blastopore.
The venous ring has been replaced by the main venous trunk (v) which has grown not
only longer but larger as it approaches the yolk stalk. With its many lateral branches,
the vitelline venous system much resembles a tree. These veinlets receive blood from the
arterioles, and the great venous trunk brings to the growing embryo much blood laden
with food stuff.
With this brief explanation, let us now turn to Dean’s drawing showing the earliest
circulation on an egg of Chlamydoselachus found by him.
VITELLINE CIRCULATION IN THE 397MM. EMBRYO
One of Dean’s three drawings in color for the embryology of Chlamydoselachus
portrays this embryo and yolk (Figure 50, plate V). In this the artist has shown the
The Embryology of Chlamydoselachus 619
proximal portions of both vitelline artery and vein. The artery extends out from under
the head of the embryo as a single vessel until it forks narrowly into two branches before
passing over the equator of the egg. The dendritic system of vessels under the tail of the
embryo is venous and laden with food absorbed from the yolk mass. This circulation on
the upper side of the egg carrying the 39mm. embryo is essentially like that portrayed
ona flat surface by Balfour (Text-figure 30). Unfortunately there is no drawing showing
the relation of arterial and venous vessels on the opposite side of the egg of this 39-mm.
Chlamydoselachus. For this we shall have presently to go to the drawings of the 43-
mm. embryo and its yolk sac.
Arterial and Venous Trunks in the Yolk Cord.—Inspection of the yolk cord of the
39mm. embryo (Figure 51, plate V) shows that the artist has not differentiated
the trunks of artery and vein in the cord. They are not portrayed in the 43-mm.
specimen (Figure 7, plate I). In the 50mm. embryo the arterial and venous vessels are
plainly shown in the yolk stalk (Figure 9, plate I), but (as in the 39-mm. specimen) they
are not distinguished from each other. Probably they run side by side and are too small to
be shown separately in these drawings made in this small but natural size. In the 175-
mm. fishlet (Figure 11, plate I) the yolk cord cannot be seen due to the position of the
wide head. Probably it is too short for the yolk-cord trunks to be seen, as is the case in
the 390-mm. shark (Figure 49, plate V).
Yorxk-Sac CircuLaTION OF THE 43“MM. SPECIMEN
This is the only embryo and egg of Chlamydoselachus whose vitelline circulation has
previously been described. This was done by Nishikawa (1898, p. 97) who had at least
six eggs with young embryos (32-60 mm. long) but he seems not to have been aware of the
studies of his predecessors—not even of Balfour’s well-known work. Had he consulted
this author, he surely would not have made such errors as fill his page and give point to
Balfour’s remark (1885, p. 465) “The observations recorded on the subject [the circulation
of the yolk-sac in sharks] are, so far as I am acquainted with them, very imperfect, and in
most cases the arteries and veins appear to have been transposed”. What our Japanese
author wrote illustrates this point.
The circulation in the yolk-sac could be clearly traced and is reproduced in Figs. 1 and 2
[my Text-figure 4, and Figures 7 and 8, plate I]. On leaving the umbilical cord [yolk cord]
the artery and vein run in opposite directions. The former receives on its course a number of
smaller veins from the two poles of the yolk-sac, and divides finally into three main branches.
The artery runs for some distance without giving off any branch, and then divides into two
main vessels, which, after running for a short distance parallel to each other, form at last, on
the opposite side of the yolk-sac, an elongated, irregularly shaped arterial ring, from which
numerous small vessels radiate toward the periphery. The arterial ring just mentioned is still
wide apart in the embryo of 32 mm., but in one of 43 mm. its two halves almost touch each
other [Figure 8, plate I], but in other respects there is no change in the circulation.
Nishikawa’s description contains many errors. An attempt was made by the
present writer to correct these by insertions in brackets, but when done the resulting
paragraph was so conglomerate and confusing that it was discarded. It has seemed best
to quote just what Nishikawa wrote, and then to describe in my own words the cir-
620 Bashford Dean Memorial Volume
culation as shown in Dean’s drawings (Figures 7 and 8, plate I). The reader can then
compare the two statements and detect the errors.
Circulation on Dorsal Surface of Yolk Sac_—As explained above, Dean had Nishi
kawa’s figures redrawn for reproduction by lithography. It may be seen in the line
cut (Text-figure 4) and in the copy (Figure 7, plate I) that the 43-mm. fish has considerable
freedom of movement on its yolk sac, as is shown in the position of the artery under the
tail of the reversed embryo. This artery is unlike that of the 39-:mm. embryo (Figure 50,
plate V) in that it gives off on the left side one small quickly bifurcating branch, but is
like the former in that the main artery divides into two just where it passes over the
equator of the yolk mass. The venous system on the embryonic side of this egg shows
much growth and differentiation over that of the 39mm. embryo portrayed in Figure 50,
plate V. In the hinder and lower segment of this half of the yolk, the dendritic arrange-
ment of the venous system shows about as in the 39mm. embryo. But in the region just
posterior to the yolk stalk, large veins on each side empty into the main trunk.
Text-figure 31
The egg of Acanthias vulgaris in its horny case. This is the earliest figure found
portraying the embryo and its vitelline circulatory system. For explanation see
caption to Text-figure 30.
After Leydig, 1852, Fig. 6, pL Il.
~ The oldest figure known to me portraying the circulatory system of a shark (Acan-
thias vulgaris=Squalus acanthias) is that by Leydig (1852, Fig. 67, pl. III) shown in my
Text-figure 31. Here the vitelline artery branches at the edge of the blastoderm and
forms the arterial ring (his “sinus terminalis”), which gives off many branches behind.
These communicate with the developing venous system whose main trunk enters the
yolk stalk from the rear. This figure portrays a circulation intermediate between that of
Dean’s 39- and 43-mm. embryos.
Circulation on Ventral Surface of Yolk The blood-vascular system on the ventral
(lower) side of the egg carrying the 43-mm. embryo will now be considered. It is un-
fortunate that there is not at hand at least one figure showing in an earlier stage the
development in Chlamydoselachus of the yolk-vascular system on this side of the egg. As
shown in Figure 8, plate I, the bifurcating vitelline artery, just below the equator of the
egg, has formed the arterial ring, which shows a number of striking irregularities. The
The Embryology of Chlamydoselachus 621
ring has contracted until now only about one-fifth the area of the yolk mass is not covered
by the arterial system. The ring gives off a multitude of branches or small arteries on its
outer side. These communicate by capillaries with the forming venous system as
Figure 8 shows. As may be seen on the lower side in Figure 8, all the veins on this side
of the ring are gathered to form the great vein entering the yolk stalk under the tail of the
fishlet—if it were drawn in its normal position. The small veins formed on the upper
side of the arterial ring (Figure 7) empty from both sides into the main vein just before it
enters the yolk stalk.
VITELLINE CircuLaTION OF THE 50-mM. EmMBryo
Since this little fish is but 7 mm. longer than the 43-mm. specimen, its yolk-vascular
system might be expected to be in about the same stage of development. However, on
the dorsal surface (Figure 9, plate I), the artery, which is under the tail of the rotated
embryo, shows six small branches before its main trunk passes over the equator of the egg
to form the normal bifurcation. The venous system on the upper side of this yolk is far
better developed than that of the younger embryo (Figure 7, plate I), the whole hinder
surface of the egg being thickly covered with small veins.
In ventral aspect (Figure 10, plate I), it is seen that the arterial ring is in about the
same stage of development as is that of the 43-mm. specimen (Figure 8, plate I). Notable
is the fact that the irregularities of the two rings are almost identical. Here there is the
same profusion of small arteries radiating outward from the ring, but not a single one
on the inside.
So far as I can find, the earliest portrayal of the closing arterial ring on the ventral
surface of an elasmobranch egg was made by Wyman (1867, Fig. 3, plate 1). On the yolk
of a rapidly developing embryo of Raia batis in the selachian stage, the ring has nearly
closed, and the yolk-sac circulatory system is in about the stage of that shown in Dean’s
Figures 9 and 10, plate I, for the 50-:mm. Chlamydoselachus.
Yorx-sac CIRCULATION OF THE 175-MM. FisH
Little can be seen of this on the dorsal side of the egg (Figure 11, plate I). Venous
blood vessels seem to cover this side of the yolk pretty thoroughly. On the fish’s right is
a large vein which may be the principal one going into the yolk stalk. On the ventral
surface (Figure 12, plate I), it is shown that the arterial ring is breaking up. Only parts of
the original artery are seen and these for the first time give off branches on the inside of the
ring as well as on the outside. The yolk-sac circulatory system of the 175-mm. embryo has
plainly reached a high stage of development, and the growth of the little fish must
go forward much more rapidly than ever with the incoming of larger amounts of
food materials.
VITELLINE CIRCULATION OF THE 390-MM. SHARK
Compared with the circulatory system of the 175-mm. shark, this stage is noteworthy
for the complete absence of the arterial ring. We see extending out under the head of the
fish one long arterial trunk which breaks up into a multitude of branches. Hence it is
622 Bashford Dean Memorial Volume
a reasonable conclusion that the disintegration of the ring, seen in process of going to
pieces in Figure 10, plate I, has gone on to completion. Not enough of the venous system
is shown to justify description.
Although, as stated above, I have never been so fortunate as to study the progressive
development of the yolk-vascular system on an elasmobranch egg, I have done so on
the large-yolked 20-mm. egg of the gaff-topsail catfish, Felichthys felis. Here was found the
same artery coming out from under the head of the embryo, bifurcating to form the arterial
ring. Then a venous system developed as in the sharks,with a main trunk coming in under
the tail of the embryo. The closing of the arterial ring was very like that in elasmobranchs.
THE ADULT CHLAMYDOSELACHUS ANGUINEUS
At the head of Dean’s “List of Figures” is this notation, “Adult—natural color”
and on the line below ““Adult—photo of head, lat. & ventral”. The photographs
—old, dark, and faded—I find. But, instead of a drawing of an adult in “natural color”,
I find drawings of two adults—a male and female shown in lateral aspect—and two draw-
ings of the head, in dorsal and ventral aspects. The drawing of the head in lateral aspect
was not needed since both adults were portrayed in this position. Presumably these
specimens are shown in “‘natural color”.
These figures are all reproduced on plate VI, which has been reserved for the adult
stage. With the reproduction and description of these drawings, the life history of
Chlamydoselachus anguineus as portrayed in Dean’s drawings and recorded in his frag-
mentary notes will have been adequately figured and followed, and we will then have seen
how correctly Samuel Garman named it the cloak-gilled snake-like shark.
AN ADULT FEMALE FRILLED SHARK
Such a Chlamydoselachus is portrayed in what is presumably natural color in Figure
52, plate VI. There is no record of its length and no indication as to the scale on which
this figure is drawn. The original drawing measures 603 mm. to the broken-off tip, and
with the tip completed—614 mm. (24.2 in.). A glance at the plate shows that the
drawing of the female (614 mm.) is longer than that of the male (538 mm.) by 76 mm.
(about 3 in.). This is to be expected. The female (shark or bony) fish is generally larger
than the male. Gudger and Smith (1933, pp. 262-263, Tables IV and V) were able to
record the lengths of 35 female specimens of Chlamydoselachus ranging from 610 to 1960
mm. (24 to 77.2 inches)—and averaging 1532 mm. (60.3 inches). They could find measure-
ments for only 15 males. These ranged from 920 to 1650 mm. (36.25 to 65 inches) and
averaged 1293 mm. (50.9 inches). However, one has to see the tables (Article V. of this
volume, pp. 262-263) to have it made clear that the females uniformly run larger than the
males. The largest male measured 1650, the next one but 1474mm. There are 16 females
ranging between these limits of the males, and there are 10 females ranging between
1670 and 1960 mm. The females average considerably larger than the males. This is
The Embryology of Chlamydoselachus 623
because the females must have body and blood to manufacture the huge ovarian eggs,
and must have a larger body-space to carry during the long gestation period the 8 to 12
eggs and embryos such are as portrayed in Figure 49, plate V.
A mere glance at Figure 52, plate VI, shows a long and slender shark whose head
and body from snout to pelvic fin are of approximately the same diameter throughout.
This uniform size of body surely enables Chlamydoselachus to creep through the inter-
stices of debris at the bottom of the sea that would stop any other shark and almost any
large teleost other than an eel. Possibly this very slender body is connected with the
feeding habits of the shark. However, this slender appearance must be considerably
changed when the fish is gravid or when the ovaries contain nearly ripe eggs (Text-figure
7). This slenderness of the body will be emphasized by giving some ratios of total length
to depth. Thus a male 1473 mm. long was in length 16.4 times the depth of the body.
A non-gravid female 1910 mm. long gave a ratio of 11.5 to 1. A 920-mm. female gave
a ratio of 12.3 to 1—a fair average between the other two. A female measuring 1860 mm.
was judged from the figure to be gravid. Her ratio was 7.7 tol. Lastly a figure of a full
bellied female, also presumably gravid, from measurements of the figure gave a ratio of
6.67 to 1.
Let us now go more into the details of the external form of our fish as seen in ‘Riguie
52, plate VI. The eye is round but the socket is somewhat distorted by the mouth being
drawn gaping. The mouth is nearly terminal and the gape is very large in both vertical
and horizontal measurements. The briar-like teeth are faintly indicated, but even plainer
are the denticles on the lips and the plications in the skin at the angles of the jaws. The
gill-covers are frilled, the frills being due to the points of the branchial rays which aid the
covers in respiration. The gill-covers of the first pair are continuous across the isthmus.
Where the covers are attached to the body are the curious curved surfaces noted in the
embryos. Visible are the ends of the gillfilaments. Surely Chlamydoselachus is
the “‘fringe-gilled”’ shark.
The back of this fish is nearly straight from the top of the head to the insertion of
the dorsal fin. On head and cheek are some of the sensory canals and on the side of the
body runs the lateral line, normal throughout—including the customary irregularity
under the dorsal. The abdomen looks full and leads to the suspicion that this female is
possibly gravid. Along the ventral surface of the abdomen are the curious tropeic folds
probably functioning as bilge keels. These keels end between the pelvic fins and immedi
ately in front of the cloacal aperture.
At the junction of trunk and tail and just in front of the caudal fin are the dorsal
and anal fins set in a vertical line. Concerning this interesting concentration of the fins of
Chlamydoselachus, Gudger and Smith (1933, p. 296) have this to say: “The close as-
sociation of dorsal, anal and pelvic fins with the caudal gives the creature a fulcrum on
which to straighten its body in striking forward to seize its prey. This was first suggested
by Garman. In ordinary swimming, right and left strokes of the caudal will send the body
forward with the sinuous motion common to all slender fishes.”
624 Bashford Dean Memorial Volume
AN ADULT MALE CHLAMYDOSELACHUS
An adult male frilled shark is accurately portrayed in Figure 53, plate VI. In the
original drawing, this figure is 538 mm. (21.2 in.) in total length. From the fact that this
drawing shows the mouth closed, one gets a clear idea of the great length of the jaws
which reach to a point well behind the rear of the skull. For measurements of the jaws of
four adult specimens of Chlamydoselachus, see Gudger and Smith (1933, p. 268). The
extraordinary structure and functioning of the jaws of this shark have been admirably
characterized by Goodey (1910, p. 550) as follows:
Perhaps the most important point in regard to the specialization of the skull of Chlamydo-
selachus is to be seen in the extreme length and mobility of the jaws. These are exceptionally
long, extending from the anterior, almost terminal mouth to a point well behind the posterior
limit of the cranium. This extension is remarkable; in fact, one quarter of the total length of
the jaws is found in this region, and it is this feature, connected with the exceptional length
of the hyomandibular, which gives the jaws their great mobility. Indeed, their disposition
relative to the cranium is quite different from that found in any other Selachian whose skull I
have been able to examine or to see a figure of. It resembles nothing among the Vertebrates
so much, perhaps, as the general disposition of the jaws in certain of the Ophidia.
As seen in Figure 53, plate VI, in the front of the mouth are a few teeth, and above
and slightly lateral is the vertical nostril with two divisions—the upper for ingress and the
lower for egress of water. The gill-covers are normal, and it can be seen that the first pair
flare widely and are continuous across the throat. Short external gill-filaments are seen
in every slit as in the female on this plate. The lateral line runs straight back to the re-
gion of the dorsal fin where the usual (normal?) irregular bendings are found. The body
cavity of the male is plainly not nearly so large as that of the female, nor is the tro-
peicfold region so well marked. On the other hand, the myomeres in the body of the
male are distinct whereas none are shown on the trunk of the female.
The above are, however, but minor differences. The one particular thing, that at
a glance differentiates this and all other male individuals from the females, is the presence
of the myxopterygia or claspers. As shown in Figure 53, plate VI, these are grooved
finger-like modifications of the hinder and inner parts of the pelvic fins. When the male
inserts these into the cloaca of the female during copulation, he holds her fast for the
passage of the spermatozoa. It is not necessary here to go further into the structure and
function of these organs. These matters have been treated earlier in this article. This
drawing is the best representation of the male Chlamydoselachus ever published.
There is another structure in which these particular drawings of the two sexes
differ—i.e., in the end of the caudal fin. In the female the tail and tail fin—as properly
restored—end in a fine point. And so do the caudal fins of most of the embryos studied.
On the other hand the drawing of the tail fin of the adult male ends in a rounded point
and there is a notch near the tip of the ventral lobe. Thus from these figures one might
jump to the conclusion that the female fish have pointed caudals and the males notched
ones. But this is not true. Gudger and Smith (1933, pp. 293-297) have gone rather fully
into the question of the form of the tip of the tail in the frilled shark, reproducing every
The Embryology of Chlamydoselachus 625
published figure of an adult Chlamydoselachus, and recording its form in their own four
specimens. But, unfortunately, they did not record the sex of each fish noted. This
I have done for all the specimens figured by them. Of these, 2 males and 4 females have
pointed tails, and one female has a tail that appears to be notched. Of the 6 adult speci-
mens in the Museum collection (4 used in previous researches, and 2 found since), all—2
males and 4 females—have pointed tails, 3 straight and 3 drooping.
THE HEAD OF THE ADULT SHARK
The lateral aspect of the head of Chlamydoselachus in both sexes, and with mouth
open and shut, is admirably portrayed in Figures 52 and 53, plate VI. What are needed to
make the portrayals complete are drawings of the dorsal and ventral aspects. Dean’s
“List” for “Adult” calls for “‘photo of head lateral and ventral”. These I find, but I also
find two excellent drawings of the adult head seen from above and below. They will
now be described. There are no notes for these as there are none for the photographs.
HEAD—DORSAL ASPECT
The head in dorsal view is shown in Figure 54, plate VI. From the angle of the
jaws, the head narrows gradually to the rounded blunt snout—a marked contrast to
the broad blunt snouts of the tiger and whale sharks and to the keen-pointed ones of the
Isurid sharks. The eyes are set in shallow cavities. From the angle of the jaws, the head
widens to its maximum over the hinder edge of the first gill-cover. In all the gill slits,
except the last, short external filaments are visible—as they are in the specimens repre-
sented in the full-length drawings. Whether or not this head is that of the male fish,
portrayed in lateral view in Figure 53, plate VI, cannot be said, but it certainly is not that
of the female fish of Figure 52 on the same plate. Her first gill-cover looks as if it had the
edge bitten off. Also the space between the first and second arches is much wider than
that between the second and third, etc. In Figure 54, the widths of the openings are very
uniform save for the last ones at the bases of the pectoral fins. These fins are entirely
normal. Running along the back on either side is the lateral line. Of the latero-sensory
head canals, nothing can be seen save one curving gracefully in front of each first gill-
cover. No spiracle is shown. The opening was probably so small that the artist did not
find it. That this head seen in dorsal aspect is that of an adult Chlamydoselachus may
be judged by comparing it with the head of the 175mm. specimen portrayed in dorsal
view (Figure 11, plate 1).
HEAD—VENTRAL ASPECT
The ventral aspect of this same head (the figures have the same measurements) may
be seen in Figure 55, plate VI. Above and on either side of the mouth, the nostrils show
faintly. The almost terminal mouth, with some of the upper teeth showing, is very
prominent. So great is the front-to-back gape, that the angle of the mouth is a little
further than halfway back of the median point between tip of snout and hinder edge of the
first gillcover. The throat has the skin plicate to allow for expansion when large objects
are swallowed. The gill-covers of the first arch are confluent across the isthmus or throat
626 Bashford Dean Memorial Volume
—i.e. the shark is cloak-gilled (Greek, Chlamys, a cloak). Paired latero-sensory canals are
found on each first gill cover and extend far on the throat region toward the symphysis of
lower jaw. The hindmost of these canals are continuations of the ones seen on the first
pair of gill-covers in the dorsal aspect. The short gill-filaments are visible.
The stout pectoral fins with their strong bases look “finished”. Beginning between
them and extending backward are the tropeic folds or bilge keels with their deep median
groove. One wishes that this excellent drawing portrayed the ventral surface clear
back to the tip of the caudal fin.
As noted, Dean’s “List” calls for ““Adult, photo of head lat. & ventral”. These
I have found, old and faded. The specimen, from which these photographs were made, had
been mutilated in both gillregions—the parts of particular interest just here—and ap-
parently had suffered partial maceration. Furthermore, the shrunken gillflaps and the
distorted gill filaments indicate that they had undergone considerable drying. These
photographs portray gill region conditions unlike what are found in the eleven figures of
heads and of whole fish reproduced by Gudger and Smith (1933). Such conditions were
not found in a single one of the six specimens in the American Museum studied by Smith
(1937), nor are they portrayed in any of Dean’s four figures reproduced herein as plate VI.
It is evident that the photographs do not portray a normal specimen as it appeared in life
and that they possess no scientific value whatever. There are no notes to tell us by whom
they were taken, why they were made, nor why they were included in Dean’s records.
They will not be reproduced in this article.
EXTERNAL GILL FILAMENTS IN CHLAMYDOSELACHUS
Before concluding this study of the breeding habits and external embryonic develop-
ment of Chlamydoselachus, the matter of its external gills must be taken up. These, as
indicated above, are commonly found in the embryos but very rarely in adults. In the
embryos they are in origin totally unlike the external gills found present in Crossopterygu,
Dipnoi, and in Amphibia, and are considerably different in length and profusion from the
external gills figured and described in the embryos of many species of elasmobranchs.
Chlamydoselachus is the only shark known to me to possess in the adult stage, even occa-
sionally, short external gill filaments. This matter of external gill flaments is so important
that it must be considered carefully.
EXTERNAL GILL-FILAMENTS OF THE EMBRYOS
The embryos of all non-placental viviparous sharks and rays known to me have long
external gills. The eggs of these elasmobranchs have thin diaphanous shells, through
which uterine fluids readily penetrate. These fluids are milk-like secretions of the uterine
mucosa and serve as food for the growing embryos, which absorb this food through their
long filamentous gills. It has been indicated above that the relatively thick shells of
Chlamydoselachus are burst by the growing embryo, are cast off into the uterus (Figure 11,
The Embryology of Chlamydoselachus 627
plate I), and are then or later thrown out into the sea. Two investigators (Hawkes, 1907;
and Smith, 1937), have found highly vascularized areas in the wall of the right uterus.
These observations suggest that these areas might have served to secrete food stuffs into
the uterus. Then the long gestation period and the enormous size of the relatively late
embryos still attached to large yolk sacs seem to indicate that these embryos grow not
at the expense of the yolk alone. All these things lead to the inevitable question—‘“Do
the external gills of the embryos of Chlamydoselachus serve to absorb food from a uterine
secretion?” The facts and inferences as to such a possible source of food in Chlamydo-
selachus have been set forth above. It seems quite sure that in any case, these external
gills of the non-extruded juvenile sharks serve as respiratory organs.
Chlamydoselachus has been ranked by the systematists as the lowest, most primitive
living shark. Yet in its reproductive organs, as this paper shows, and in many other
organs, as Smith has pointed out in his monograph on the anatomy (1937), it is very
highly specialized. Its embryos have external gill-filaments, which never grow very long
and which eventually shorten until they are almost or quite concealed from view by the
gill flaps. Now external gills, as they are ordinarily understood, are embryonic or an-
cestral organs which tend to become eliminated in the process of evolution. External
gill filaments are either evanescent structures of external origin, developed as outgrowths
on the outermost edge of a visceral arch before the clefts have broken through, or they
are precocious growths of normal gills which tend to shorten in the course of later de-
velopment. Let us now study these filaments as they are shown in the drawings of the
embryos of this archaic shark and see to which category they belong.
The first evidence of the presence of gillfilaments in the embryos of Chlamydo-
selachus is found in the 25-mm. stage as portrayed by Ziegler (1908, Fig. 2). Ziegler’s
figure (my Text-figure 27c) is poorly reproduced on soft paper, and the budding filaments
show up indistinctly. However, in the figure these buds appear not on the outer edges of
the gillarches but on the hinder inner sides of arches 1-5, and on both sides of No. 6.
Furthermore, it is clear that the gill-clefts have become perforated, and that the outside
liquid penetrates into the pharynx through the slits.
Brohmer’s drawing (1909, Fig. 3) of his 25-mm. specimen (also poorly reproduced)
shows the gill-filament buds on both sides of arch No. 2 (my Text-figure 274). Probably
they are present in a beginning stage on both sides of each arch. They are next seen (as
far as data are at hand) in Nishikawa’s 32-mm. embryo (Figures 19-21, plate II) where
they appear on both sides of every arch—excepting of course the first. Passing over the
34-mm. specimen, we go to the 39-mm. embryo in which stage the filaments first begin to
show externally, particularly in the first slit (Figure 25, plate II). These filaments are in
about the same stage of development as those in Scammon’s 18mm. Squalus (1911, Fig.
27, pl. II). But in size and abundance they are far behind the filaments protruding from
the gill-slits of Scammon’s 20.6-mm. embryo of the dogfish.
External filaments are seen to be pretty well developed in Dean’s “new series” of
drawings of embryos 46, 54, 66, and 103 mm. in length. These can be best studied in the
628 Bashford Dean Memorial Volume
ventral views reproduced in Plates III and IV. where they seem to be growing on both
sides of each slit. That this is a fact, I have proved by microscopic examination of the
head of an embryo about 45-mm. long found in the Dean material in the Museum. This
specimen had been fixed in bichromate of potash and under the binocular microscope
showed filaments on both the anterior and posterior sides of every arch save the hyoid—
and some protruded even from the spiracle. These external filaments are somewhat better
developed in the 103-mm. fish (Figures 41-43, plate IV) than in any younger embryos.
But even here they are hardly so well-grown as those in Scammon’s 20.6-mm. Squalus
(his Fig. 28, tab. III).
Among the embryos loaned from Columbia University for this research, I could for
a long time find no specimen with gillfilaments longer than those of the 46mm. young
(Figures 28-30, plate III) and of the 103-mm. fish (Figures 41-43, plate IV). However,
one day in examining the egg with the split yolk (referred to previously) as having a cap-
sule with the curious tendriliform process seen in Figure 13, plate I, I removed the crum-
pled shell, and to my great surprise and pleasure found the little fish with long filaments
now to be studied.
This specimen (71-mm. long), as seen in Text-figure 32, has longer and more profuse
external gillfilaments than any young Chlamydoselachus figured by Dean. This will be
noted at once when Text-figure 32 is contrasted with Figure 41, plate IV (the 103-mm.
specimen). It is impossible to measure these filaments since they are more or less sinuous,
and sometimes spirally coiled. Due to their being tangled, they sometimes appear to be
branched, but under the binocular microscope this is seen to be an optical illusion due to
their overlying each other. For comparison’s sake, there is introduced here, as Text-figure
33, Scammon’s figure of his 28mm. Squalus in about the same stage of gill-filament
development as the 71mm. Chlamydoselachus. Possibly if the filaments of the little
Text-figure 32
A 71-mm. frilled shark with a profusion of external gill-filaments. These are the longest found in any
specimen or drawing of this shark in this research.
Photograph by Charles H. Coles, A. M. N. H.
The Embryology of Chlamydoselachus 629
Text-figure 33
A drawing of a 28-mm. Squalus acanthias in about the same stage of external gill filament develop.
ment as is the young Chlamydoselachus shown in Text-figure 32.
After Scammon, 1911, Fig. 30a, Pl. III.
frilled shark could be straightened out they might be as long as those of the dogfish. The
two little sharks are shown in the same size, though in life Chlamydoselachus is 2.5 times
longer than Squalus. This shows how much faster and farther the dogfish had gone in
development. For a frilled shark of approximately the same size as this Squalus, see
Figure 23, plate II of a 34-mm. Chlamydoselachus.
In Dean’s figures of older embryos measuring 124, 175, 185, 240, and 390 mm., and
all drawn at an earlier date then those of 46, 54, 66, and 103 mm., the external filaments are
very much reduced. They are hardly visible underneath the flaps. From all the data
carefully marshalled above, I draw the conclusion that these so-called external gills of the
larval frilled shark are nothing but precociously overgrown permanent gills, which later on
shorten until but a bare remnant shows beyond the gill-opening, as may be seen in the
largest (390-mm.) embryo portrayed by Dean (Figure 49, plate V).
From these facts, found in the drawings cited, it is clear that these protruding gill-
filaments in the embryos of Chlamydoselachus are not true external filaments like those
of the Crossopterygii, Dipnoi, and Amphibia. In the larvae of the dogfish and of the
various rays dissected and studied by me, the external filaments are many, long, and plu-
mose. By the time of hatching these have disappeared. Whatever may be the part of
these external gills in the nutrition and respiration of the embryo, they are almost always
absent in the adult.
EXTERNAL GILL-FILAMENTS IN THE ADULTS
No other adult shark or ray known to me has even the semblance of external gills,
but some specimens of the adult Chlamydoselachus do have such a semblance. Allis
(1923) has a drawing (reproduced by Gudger and Smith, 1933, in their Fig. 7, pl. I —
Article V of this Memorial Volume) made from an adult head supplied to him by Dean,
which shows such remnants of protruding filaments as are seen in Dean’s figures on
630 Bashford Dean Memorial Volume
Plate VI. Allis’s figure in his article (1923) appears to be in natural size, and Dean’s
figure of a female fish in the original drawing measures 614 mm. (24.2 in.). This, it should
be noted, is just about the size of a young specimen taken by the Prince of Monaco at Ma-
deira, and pronounced by Collett (1890) to differ from adults only in the matter of size.
Elsewhere it has been stated that there are in the Museum collection six adult
frilled sharks. What is the evidence from them as to protruding gill filaments? Three of
these sharks have been dissected by Smith (1937) who found that the gillflaments did
not show externally. Similar conditions were found in the three undissected specimens.
None showed protruding filaments. We also havea head only, straight and well-preserv-
ed, but it shows no external filaments. As to the function of these slightly protruding
gill filaments, one can infer that they make the gills of such adults as possess them, some-
what more efficient in respiration.
From the data given, it is probable that some embryos of Chlamydoselachus (Fig-
ure 49, plate V) carry over into the adult stage remnants of their embryonic external gills.
But it is evident that most adults lack such protruding gill flaments. For figures in which
they are absent, see Gudger and Smith’s (1933) article on the natural history of Chlamydo-
selachus, wherein all known figures of the whole fish and of its head are reproduced. That
external gills sometimes occur in the adult Chlamydoselachus is additional evidence of the
unpredictable characteristics of this primitive shark. Perhaps I cannot do better than to
quote Smith’s summation (1937, p. 495)—‘My outstanding impression of the frilled
shark is that it presents a strange assemblage of characters ranging from very primitive to
highly differentiated”.
The Embryology of Chlamydoselachus 631
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n. s. 17, 487.
1904. A visit to the Japanese zoological station at Misaki. Pop. Sci. Monthly, 65, 195-204, figs.
Detneca, W. A.
1925. On the abdominal viscera of Chlamydoselachus anguineus Garm. (Russ. text, Eng. summary).
Bull. Soc. Nat. Moscou, (Sect. Biol.), n. s. 34, 194-206, 3 figs.
Dortetn, Franz
1906. Ostasienfahrt: Erlebnisse und Beobachtungen eines Naturforschers in China, Japan und
Ceylon. Leipzig. (Data on Chlamydoselachus, pp. 257, 267-268, fig.)
632 Bashford Dean Memorial Volume
GarMANn, SAMUEL
1885. Chlamydoselachus anguineus Gar.—a living species of cladodont shark. Bull. Mus. Comp.
Zool., 12, 1-35, 20 pls.
GARMAN, SAMUEL
1913. The Plagiostomia (sharks, skates and rays). Bull. Mus. Comp. Zool., 36, (Eggs and embryos of
Chlamydoselachus anguineus: pl. 59, figs. 4 and 5; pl. 61, figs. 7 and 8.
Goopry, T.
1910. A contribution to the skeletal anatomy of the frilled shark, Chlamydoselachus anguineus Gar.
Proc. Zool. Soc. London, pt. 1, 540-571, 5 pls.
Gupeer, E. W.
1912. Natural history notes on some Beaufort, N. C. fishes, 1910-11. No.1. Elasmobranchii—with
special reference to utero-gestation. Proc. Biol. Soc. Washington, 25, 141-156.
1913. Natural history notes on some Beaufort, N. C. fishes—1912. Proc. Biol. Soc. Washington, 26,
97-110.
1918. Oral gestation in the gaff-topsail catfish, Felichthys felis. Papers Dept. Marine Biol., Carnegie
Instit. Washington (Pub. no. 252), 12, 25-52, 4 pls.
Gupcer, E. W. anp Situ, B. G.
1933. The natural history of the frilled shark, Chlamydoselachus anguineus. Bashford Dean Mem.
Vol.: Archaic Fishes, Art. V, pp. 243-330, 5 pls. and 31 text-figs.
Haswett, W. A.
1897. On the development of Heterodontus (Cestracion) phillipi. Proc. Linn. Soc. New South Wales,
22, 96-103, 2 pls.
Hawkgs, O. A. Merritt
1907. On the abdominal viscera and a vestigial seventh branchial arch in Chlamydoselachus. Proc.
Zool. Soc. London, 471-478, 3 figs.
LeicH-SHARPE, WILLIAM HaroOLp
1922. The comparative morphology of the secondary sexual characters of elasmobranch fishes—the
claspers, clasper siphons, and clasper glands. Mem.I. Journ. Morphol., 34, 245-266, 12 figs.
Leypic, Franz
1852. Beitrage zur mikroskopischen Anatomie und Entwickelungsgeschichte der Rochen und Haie.
Leipzig. (Embryologischer Teil, pp. 90-120, pls. III and IV).
LoHBERGER, JOHANNES
1910. | Ueber zwei riesige Embryonen von Lamna. Abh. Bayer. Akad. Wiss., Suppl. Bd. 4, (Beitrage
zur Naturgeschichte Ostasiens, Abt. 2, 45 pp., 5 pls).
Momosg, F.
1938. A newly arrived specimen of the “‘Frilled Shark” [text in Japanese]. Natural Science and
Museum, Tokyo, 9, (no. 8), 2-5, 7 figs.
NisHIKAWA, T.
1898. Notes on some embryos of Chlamydoselachus anguineus Garman. Anmnot. Zool. Japon., 2,
95-102, pl., 3 text-figs.
Ospurn, RayMmonp C.
1906. The origin of vertebrate limbs. Recent evidence upon this problem from studies on primitive
sharks. Ann. New York Acad. Sci., 17, 415-436.
1907. | Observations on the origin of the paired fins of vertebrates. Amer. Journ. Anat., 7, 171-194,
5 pls.
The Embryology of Chlamydoselachus 633
Rosg, C.
1895. Ueber die Zahnentwicklung von Chlamydoselachus anguincus Garm. Morph. Arb., 4, (A 340-
mm. embryo im Leibe of a female Chlamydoselachus, p. 194).
Sanzo, Lulci.
1910. | Embrione di Carcharodon rondeletii M. Henle, con particolare disposizione del sacco vitellino.
Mem. R. Comit. Talassog. Ital., no. 11, 1-10, 2 pls.
ScamMmon, RICHARD E.
1911. Normal plates of the development of Squalus acanthias. In Keibel. F. Normentafeln zur
Enwicklungsgeschichte der Wirbeltiere. Jena. Heft 12, 140 p., 4 pls., 26 text-figs.
SHANN, Epwarp W.
1910. A description of the advanced embryonic stage of Lamna cornubica. 28. Ann. Rept. Fishery
Board Scotland, pt. III, Sci. Invests., 73~79, pl.
Smit, BertraM G.
1937. The anatomy of the frilled shark, Chlamydoselachus anguineus Garman. Bashford Dean Mem.
Vol.: Archaic Fishes, Art. VI, 331-520, 7 pls., 128 text-figs.
VAILLANT, L£on
1889. Note sur un foetus gigantesque d’Oxyrhina spallanzanii Bonap. Bull. Soc. Philomath. Paris, 8.
ser. 1, 38-39.
WYMAN, JEFFRIES
1867. Observation on the development of Raia batis. Mem. Amer. Acad. Arts and Sciences. n. s. 9,
31-44, pl.
Ziecuer, H. E.
1902. Lehrbuch der vergleichenden Entwickelungsgeschichte der niederen Wirbeltiere. Jena. (Sela-
chier. pp. 101-152, 55 figs.).
Ziecuer, H. E.
1908. Ein Embryo von Chlamydoselachus anguineusGarm. Anat. Anz., 33, 561-574, 7 figs.
ALANIS, II
EXTERNAL DEVELOPMENT OF CHLAMYDOSELACHUS
BD gs &
PLATE I
EGGS AND EGG CAPSULES OF CHLAMYDOSELACHUS
A ripe ovarian egg of the frilled shark. The original drawing measures 90 x 96 mm., and is pre-
sumably in natural size. See also Text-figure 12.
An asymmetrical oblong egg of the frilled shark. The asymmetry of this egg probably originated
during the process of shell formation.
A symmetrical oblong egg of Chlamydoselachus surrounded by its transparent keratinoid capsule.
A round egg of the frilled shark—C of Dean’s list.
Another encapsuled round egg—numbered B by Dean.
A third round egg—numbered A by Dean.
An ellipsoidal encapsuled egg having a 43-mm. embryo attached by a yolk stalk.
This figure is a copy of Nishikawa’s drawing portrayed in natural size in Text-figure 4.
The vitelline blood vessels on the under side of the egg portrayed in Figure 7.
After Nishikawa, 1896, Fig. 2, pl. IV.
An ellipsoidal encapsuled egg with an older embryo (50 mm.) and a slightly more advanced vitelline
circulation than that seen in Figure 7.
Underside of the egg shown in Figure 9. The yolk-sac circulation is slightly more advanced than
that portrayed in Figure 8.
A 175mm. embryo of Chlamydoselachus attached to its yolk sac and without its capsule.
Under side of egg portrayed in Figure 11. This shows a late stage of the vitelline blood vessels.
A tendriliform process from the capsule of an asymmetrical oblong egg in the collections of Co-
lumbia University. This process is similar to that seen in Figure 2.
A much-branched tendriliform process. Note its close similarity to those shown in Figures 13
and 2.
Each figure on this plate save number 13 is half the size of the original, and hence is presumably one half natural size.
Figure 13 is the only figure on these six plates not drawn by or for Dr. Bashford Dean.
Dean MemoriaAt Votume z ARTICLE VII, Prate I.
=
eS.
are ae
BasHrorp DEAN DEL. A. Horn & Co. Lira.
EMBRYOLOGY OF CHLAMYDOSELACHUS
PILATE JU
EXTERNAL DEVELOPMENT OF CHLAMYDOSELACHUS
PLATE II
THE EARLIEST EMBRYOS OF CHLAMYDOSELACHUS OBTAINED
BY BASHFORD DEAN
The earliest embryo (11.5 mm.) of Chlamydoselachus figured by Dean. Original drawing =121 mm.
Note the attachment of the embryo to the yolk sac by a short yolk cord.
The 11.5-mm. embryo stained, cleared, and drawn considerably enlarged—to 161 mm.
A larger embryo (15.5 mm.) shown in lateral aspect. The original drawing measures 177 mm.
The largest (20 mm.) of Dean’s very small embryos of the frilled shark. The original drawing
measures 222 mm.
Dorsal view, head only, of Nishikawa’s 32mm. embryo, considerably enlarged.
Lateral aspect, the head only, of Nishikawa’s 32mm. embryo.
Head only of Nishikawa’s 32mm. embryo seen from below.
Dorsal aspect of head only of Dean’s 34-mm. Chlamydoselachus.
Lateral view—full-length—of the 34-mm. embryo.
Ventral aspect of the head only of Dean’s 34-mm. specimen.
Dean’s 39-mm. embryo portrayed in full-length lateral aspect.
All the figures on this plate are reduced by one-third—i.e., are reproduced
two-thirds the sizes of the original drawings.
Basurorp DEAN DEL.
EMBRYOLOGY OF CHLAMYDOSELACHUS
ARTICLE VII, Pare IT.
——
A. Horn & Co. Lirn.
Bes 100
EXTERNAL DEVELOPMENT OF CHLAMYDOSELACHUS
PLATE Il
FRILLED SHARK EMBRYOS OF INTERMEDIATE SIZE:
39, 46, 48. 54. 55 MM.
An embryo of 39-mm. portrayed in full-length dorsal aspect.
Ventral view—full-length—of the 39-mm. specimen.
Full-length portrayal in dorsal aspect of a 46-mm. embryo.
Lateral full-length view of the 46-mm. embryo.
The 46-mm. embryo seen from below.
“Head only stained” of a 48mm. embryo—ventral aspect.
A 54mm. embryo shown in full-length dorsal view.
A fulllength lateral view of the 54mm. fishlet.
The tadpole-shaped 54mm. embryo portrayed from below.
Dorsal aspect—head only—of a 55-mm. embryo.
Lateral full length view of a 55-mm. specimen.
Head only of a 55-mm. embryo seen from below.
All figures on this plate have been reduced by one-third their original length.
os
BasHrorp DEAN DEL.
EMBRYOLOGY OF CHLAMYDOSELACHUS
ArticLe VII, Prater III.
A. Horen & Co. Lirn.
PEATE SY)
EXTERNAL DEVELOPMENT OF CHLAMYDOSELACHUS
Fig.
Fig.
So
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
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Fig.
Fig.
Fig.
PICANIUE, IINV/
LARGER EMBRYOS OF CHLAMYDOSELACHUS:
66, 103, 124, 185, 240 MM.
Dorsal view—full-length—of a 66-mm. embryonic Chlamydoselachus.
A 66mm. embryo of the frilled shark seen from the left side.
Ventral aspect of the 66mm. specimen.
A specimen 103 mm. long viewed from above.
A 103-mm. embryonic frilled shark seen from the side.
A young 103-mm. Chlamydoselachus in ventral aspect.
Head of a 124-mm. embryo seen from above.
A 124mm. Chlamydoselachus portrayed in lateral aspect.
Lateral view of an embryo 185 mm. long.
Head only of the 185-mm. embryo—ventral aspect.
An embryo measuring 240 mm. seen in lateral view.
All the figures on plate IV. are reproduced two-thirds the size of the original drawings.
ArtTIcLE VII, Piate IV.
BasHFrorD DEAN DEL. A. Horn & Co. Litx.
EMBRYOLOGY OF CHLAMYDOSELACHUS
JOGA WY’
EXTERNAL DEVELOPMENT OF CHLAMYDOSELACHUS
ig. 49.
. 50.
5 Sle
IAL ANIC WY
A 390-MM. FRILLED SHARK, A 39MM. EMBRYO, AND A WIND EGG:
ALL PORTRAYED IN NATURAL COLORS
Dean’s largest (390-mm.) embryo of Chlamydoselachus portrayed in lateral view
in its natural colors.
A 39mm. embryo, its yolk mass, and its yolk-vascular system shown in natural colors.
A wind egg of Chlamydoselachus shown in its natural colors.
Figure 49 on this plate is reduced from 15.35 in. toll in. Figures 50 and 51 are reproduced in the size
of the original drawings.
Dean MemoriIAL VOLUME ARTICLE VII, Piate V.
|
4
BasSHFORD DEAN DEL. A. Hoen & Co. Lit.
EMBRYOLOGY OF CHLAMYDOSELACHUS
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EXTERNAL DEVELOPMENT OF CHLAMYDOSELACHUS
Fig. 52.
Fig. 53.
Fig. 54.
Fig. 55.
Lene, WI
| MALE AND FEMALE SPECIMENS OF CHLAMYDOSELACHUS
AND TWO HEADS FROM ADULT FISH, ALL SHOWN IN
THEIR NATURAL COLORS
Lateral view of a female Chlamydoselachus.
Lateral view of a male frilled shark.
Dorsal view of the head of an adult frilled shark.
Ventral view of the head of an adult Chlamydoselachus.
Figures 52 and 53, in the original drawings, measure 614 mm. (28.4 in.) and 538 mm. (21.2 in.)
respectively. As reproduced on this plate, the fishes measure 505 mm. (19.9 in.) and 443 mm.
(17.4 in.) each. Figures 54 and 55 are reproduced in the size of the original drawings.
Mewouat Vouse
EMBRYOLOGY OF
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BASHFORD DEAN MEMORIAL VOLUME
FENN Cavan laltslalles
Edited By
EUGENE WILLIS GUDGER
Articie VIII
THE HETERODONTID SHARKS:
wHEIR NATURAL HISTORY, AND THE EXTERNAL
DEVELOPMENT OF HETERODONTUS JAPONICUS
BASED ON NOTES AND DRAWINGS
BY BASHFORD DEAN
By BERTRAM G. SMITH
: Professor of Anatomy
New York University College of Medicine
New York City
a.
L2.MERICAN \<
MUSEUM
NEW YORK
PUBLISHED BY ORDER OF THE TRUSTEES
Issued October 1, 1942
JANRITIGHE, WALI
THE HETERODONTID SHARKS: THEIR NATURAL HISTORY,
AND THE EXTERNAL DEVELOPMENT OF HETERODONTUS
(CESTRACION) JAPONICUS BASED ON NOTES
AND DRAWINGS BY BASHFORD DEAN
By Bertram G. SMITH
CONTENTS
INIER © DUCTION ae ten eae utr ersae tte eubt crs bp neegeucnaieitn le ey mesa a eneister ain
IMATE RTA TRAN MRE CORDS ate Rere a eaen tani ae tyre ea pases Poe a te cterek ea nee eRe
SIGHT SPECIMENS PANDMISHETRYS OURCE DHE IT rear iei ai ie ereeiirloiire rey ene tener eara
/NGTORNIAD OF WB IDRAWHINEBs coavlccwavooe asd veosenenvcevsoococucu cD adoCUsGORES
Written Recorps Lert By BASHFORD DEAN....... 2... 0.000 be tee ee
CLASSIFICATION FASNIT) AVANT @INWAN Ya neta tyes Sec ears Mocca RE myn chal e.seltaite hy earn
Heterodontus/ AND) HIETERODONTIDAEL a aii ie iol ae eine ieneeia se selene sl
SYNONYMYARIC? EEO ACCOR Ie ra ee Oe eens tyeast aT remvnernek katotren suepalei and ak eet.
Commons NAMES —BULLHEADISHARKS Hem rn ena eer eichrr iste kackteieie nents ie tet Fete er para
RAMILYeANDI GENERIC] CHARACTERS HERR Ene er ene tine eimai eerste iii rites rarer
SIGHEY SPECIES OFPELeterOdONttls MEER ee en eR ee eo eis emcee eer
eterodontus)phillipis BEAINVILLE Menace eee cie eee cet incr tee ee
bleterodontusizebral G RAYA A RTE nE rn cencR Eee ner Ciencia rire terra et:
Heterodontus) quoyt FREMINVILLE® 21260020222 e oslo ole ms elie eels eee elie rt epee oe enedeierel= ier
Heterodontusipranciscia GIRARDER GEE Reer eee ee ce cite tect toe erie errr rr
Comparison oF H. quoyi AND H. francisci .... 2... 2.16 e eee ee eee
Heterodontusiedleatus| GUNTHERSTR ERE err e e Ree Rtn ce Gene cence errr eer race
Heterodontus japonicus MACLEAY. 0.22.0... oe oe ee et te ee eee me
ANNs IO JF Os JBORIVSs ooo od coco ccc oceousnoodnodebeasconvnudadeoncas
SExUAL DIMORPHISM AND THE REPRODUCTIVE ORGANS... . 22.000 00 ee ete
Tue Ece Capsutze: Its SrrucTURE AND FUNCTIONS. ........--00 020002 see eee
IPABIERSTORMELCEETOCOTIEU Ske a eric ev sy rrueT S seiaes feraNeehd tucne Mion aoc a vee: geen eee
JRLARaATE ATK iD) GUATAUNT IGIARIOSs ooo oon daenosaeveduvooopo aos ooo oOo ODOG DO De boa UDIHD
EGODPANDENEEDINGERLABLTS ee o ee ee ae a aerate
Emsryonic DevELOpMENT OF Heterodontus japonicus.........-..--++--5 +5050
RVATEIOR EMBRYONIC DEVELOPMENT) < yela sic <2. o eeen el eieet ol lie) oiler eniedts ote Peddler =)y-h ist amtent-ynometon=
WATERS EMBRY.ONICHDEVELOPMENAM erica tie ciel cits ech sei eeneeiolen tenet tb) ate Riente oid
ADHEINAATEDEINER OR CULATIONS EEE een ia oriinrinio eae ie ery rena
IATCHING AND THEVNEWLY GIATCHED) YOUNG... .-... 0005500006 > 2 > see oe
W280 MMe YOUNG Eleterodontius) ya pomicuss asa se aye ee eee cee
FE XERINAT AN DEINDERNAT | Gili) hIPAMENDS.) 6c es ier tent eicr ee e
IDENARUOMMIsINAe Oi Weis Issarets Loo a dena be oarococupesogobnsongnc coco scudans
BIBEIOG RABE Ure Hemet me iene ties eevee tal ene s WM ncaly So ale ish centres teamerccs eatyraiellsyceinteh
THE HETERODONTID SHARKS: THEIR NATURAL HISTORY,
AND THE EXTERNAL DEVELOPMENT OF HETERODONTUS
(CESTRACION) JAPONICUS BASED ON NOTES
AND DRAWINGS BY BASHFORD DEAN
By Bertram G. SMITH
Professor of Anatomy
New York University College of Medicine
New York City
INTRODUCTION
Sharks of the family Heterodontidae (Cestraciontidae) have an especially well-
defined pedigree. The genus Heterodontus (Cestracion), which includes the only species
living at the present time, dates at least from the Upper Jurassic; the family Cestracionti-
dae, as defined by Zittel (1932), from the Lower Jurassic. The closely related family
Hybodontidae, represented only by fossils, dates from the Devonian or Lower Carbonifer-
ous to the Cretaceous. Therefore the geologic histories of the two families overlap; but
the Hybodonts were approaching extinction when the Heterodonts came into being.
Since there appears to be genetic continuity between the two families, one might readily
conclude that the recorded lineage of sharks of the genus Heterodontus is more ancient
than that of any other living vertebrate. In this circumstance we find the key to Dean’s
interest in the embryology of Heterodontus.
At the time when Dean began collecting the eggs and embryos of the Japanese
Bullhead Shark, Heterodontus japonicus, all that was known concerning the embryonic
development of any species of Heterodontus was contained in Haswell’s brief account
(1898) of the blastula and gastrula of H. phillipi. This deficiency was the more notable in
view of the fact that the family Heterodontidae has no other genus, besides Heterodontus,
represented by living species. But Heterodontus was not, from Dean’s point of view,
merely another kind of shark to be studied in order to fill a gap in our knowledge of
comparative embryology. It is well known that Dean, like many other biologists of his
generation, was interested in the study of animals chiefly from the viewpoint of organic
evolution. Thus it is not surprising to find in his notebook the following carefully
worded statement:
The embryology of the Cestracionts [Heterodonts] is expected to prove of value not
merely in comparison with other sharks, but in estimating the general significance of develop-
ment in “recapitulating” ancestral characters. For granting that these sharks represent
a peculiarly primitive branch of the descent-tree of Selachians, we would reasonably expect
to find in their embryonic stages certain simpler, more archaic characters than in the cor-
responding stages of the commoner groups of sharks. Furthermore, and this is the importance
of such a study, if we do find that Cestracion [Heterodontus] presents definitely more primi-
tive embryonic characters than sharks of a more modern type, we can certainly maintain
651
652 Bashford Dean Memorial Volume
that recapitulation is not to be given the scant courtesy with which it has come to be treated
by a modern school of embryologists. In a word, the present theme may be found to provide
a new (and critical) means of testing the value of the biogenetic law.
These hopes and expectations led to the publication, in 1901, of Dean’s article
entitled ‘‘Reminiscence of Holoblastic Cleavage in the Egg of the Shark, Heterodontus
(Cestracion) japonicus Macleay.” This contribution is reviewed, in considerable detail,
later in the present paper. Our knowledge of the embryology of Heterodontus is still
incomplete, so that the possibilities suggested by Dean have never been fully explored.
To Dr. E. W. Gudger, editor of the Dean Memorial Volume, I am indebted for many
helpful suggestions throughout the preparation of this article, and especially for taking
the major part in the difficult task of making up the plates.
MATERIAL AND RECORDS
For the proper evaluation of any scientific record, it is necessary that the reader
should be informed concerning the identity, amount and source of the material, also the
Text-figure 1.
The Marine Zoological Station at Misaki, Japan.
From a photograph by Bashford Dean, 1904, p. 198.
The Embryology of Heterodontus japonicus 653
139° 5 10" 1s° 20° 25 30 35° 40° 45° 50°
1 1 . y . —— — .
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SAGAMI BAY
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5 ae 5
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Text-figure 2.
A map of the Sagami Sea, the Miura Peninsula, and part of the Gulf of Tokio, showing the position
of the Misaki Laboratory in which Dr. Dean worked, and the waters from which his specimens
of Heterodontus were taken.
From an old chart compiled by Professor I. Ijama.
After Gudger and Smith, 1933, Text-figure 3, page 251.
conditions under which the observations were made. In the present instance, this
information is not so adequate as it would be if Dr. Dean had lived to finish his projected
article on the embryology of Heterodontus japonicus; for his written TeemHES have come
down to us in fragmentary and incomplete form.
THE SPECIMENS AND THEIR SOURCE
From Dean’s notes, also from Mrs. Dean, we learn that eggs and embryos of Hetero-
dontus were obtained in Japan in 1900, 1901 and 1905, while Dean was a guest of the
Imperial University of Tokyo; also, collecting was carried on for him during his absences
from Japan, in 1903, 1904 and 1906. The material was collected at the Marine Zoological
Laboratory of the University (Text-figure 1) situated at Misaki on the Miura Peninsula
which projects into the Sagami Sea between Sagami Bay and the Gulf of Tokyo (Text-
figure 2). Collecting was done at various times throughout the year. The specimens
represented numerous stages from early cleavage to young at the time of hatching, in all
about 200 embryos. Of these, the majority were examined living, and notes and draw-
ings were sometimes made before the embryos were preserved.
654 Bashford Dean Memorial Volume
It is known that Dean, while in Japan, made extensive collections of biological
material other than Heterodontus, and that he was also engaged in the collection of
Japanese armor; but his keen interest in the embryology of Heterodontus is attested by the
following statements included in a letter (Dean, 1901.2, p. 85) to the Columbia University
Quarterly:
My frst object in visiting Japan was to secure the eggs and embryos of the Port Jackson
[sic] shark, a form which there is some reason to believe traces a direct descent from known
sharks of Carboniferous times. Its embryos, therefore, might reasonably be looked upon to
furnish evidence as to the relationships of the oldest sharks, and, therefore, as to the oldest
backboned animals. At Misaki I soon found that this form was moderately common, and the
native divers and fishermen finally brought me in a valuable series of its eggs.
In his article on the embryology of Chlamydoselachus, Gudger (1940) has noted that
Dean collected embryos of Heterodontus and Chlamydoselachus in the same general locality
(though in different habitats) and simultaneously. When we consider the results of the
two undertakings, certain differences are very obvious: whereas for Chlamydoselachus
there was a scarcity of early stages and a fairly complete series of older embryos, for
Heterodontus nearly all stages are represented. To illustrate this, one need only compare
the plates illustrating the present article with those of Gudger’s article on the Embryology
of Chlamydoselachus, No. VII in this Volume.
Of the approximately 200 embryos of Heterodontus japonicus collected by Dean,
there are now, after more than 35 years, available for study only the following: (a) Six
embryos in a crumpled condition, preserved in alcohol. Roughly measured, these range
from 38 mm. to 90 mm. in length. In general, the condition of this material is as good as
could be expected since it has been preserved for thirty-five or forty years. (b) A single
embryo about 3.5 mm. long, stained, cleared and mounted in toto on a slide. (c) Twelve
slides containing serial sections of seven different embryos in stages ranging from an
early blastula to an embryo about 10 mm. long. Several series are imperfect or very
incomplete, but the orientation is good and the stain (apparently borax carmine) has not
faded appreciably. Nevertheless, the paucity of material is such that for the embryolog-
ical portion of this article we must depend almost entirely on Dean’s notes and drawings.
Fortunately the drawings represent not only surface views, but quite a number of embryos
that had been stained, cleared, and mounted whole.
Tt was at Misaki that Dean made the only photograph of a fresh-caught Japanese
Bullhead Shark on record (my Text-figure 3, further described on page 693). This photo-
graph is particularly valuable since there is but one juvenile and no adult specimen of
Heterodontus japonicus in the American Museum at the present time. Fortunately, there
are available two specimens of H. quoyi, one young and the other adult or nearly so; and
two specimens of H. francisci, one nearly full grown and the other undoubtedly adult.
The external anatomy of all these specimens is briefly described in the section on “The
Species of Heterodontus”’.
The Embryology of Heterodontus japonicus 655
Text-figure 3.
Photograph of a fresh-caught Bullhead Shark (Heterodontus, probably japonicus) taken at Misaki, Japan.
The specimen is an adult female about 1043 mm. (41 inches) long.
After Dean, 1904, p. 203.
AUTHORSHIP OF THE DRAWINGS
Owing to the lapse of many years since the drawings of Heterodontus and Chlamy-
doselachus were made, the precise circumstances have become involved in some obscurity.
When, where and by whom were the finished drawings made? It is known that Dean was
an artist of no mean ability, and that he was skilled in the various techniques employed in
. illustrating his published works. He made pencil sketches with surprising speed and
fidelity; he had an artist’s ready perception of form and quick appraisal of light and shadow.
His more finished drawings reveal an accuracy of outline and delicacy of shading that
invariably arouse the admiration of the beholders. During his sojourn in Japan, he
had learned to use the brush in making fine lines, often in color. It is known that he had
made drawings similar to those of Heterodontus, and so it was natural that the idea should
develop among some of his friends and associates that all the drawings of Heterodontus
were the work of his own hands. But, considering the variety and the scope of Dean’s
activities, it seems physically impossible for him to have made all the drawings that
illustrate his published works, and also the drawings that were left unpublished after his
untimely death. It seems more likely that Dean often made sketches to illustrate the
character of the drawings desired, and then left the execution of the finished drawings to
artists whom he employed.
So far as Chlamydoselachus is concerned, the matter of the authorship of the draw-
ings has been fully considered by Gudger (1940) who came to the conclusion that they
were made by Japanese artists under Dean’s direction. The same considerations hold for
Heterodontus, with the following additional circumstances: The present writer remem-
656 Bashford Dean Memorial Volume
bers that in 1911 Prof. Dean showed him the plate figures of the projected article on the
embryology of Heterodontus and remarked that they were made by the best artist (or
artists?) available. I do not recall whether he stated that the artists were Japanese, but it
seems that some of the drawings bear intrinsic evidence of Japanese handiwork. A foot-
note to Dean’s article (1901.1) on the “cleavage” of the egg of Heterodontus states that
these drawings were made by Messrs. N. Yatsu and I. Kuwabara. In one of Dean’s
notebooks there is a table listing embryos of Heterodontus japonicus collected at Misaki,
and recording occasional brief data concerning them. In this table there are many
entries, in Dean’s almost microscopic handwriting, reading ““Yatsu drawn.” Whether
these drawings were preliminary sketches or figures intended for publication is not
evident from these records; but on the original of Figure 40, plate VI, there was found,
apparently in Dean’s handwriting, the word “Yatsu’”’.
After diligent inquiry it appears certain that some, at least, of the plate figures used
to illustrate the present article were made by Yatsu, and that part of his work was done in
this country. One can readily appreciate the advantages of having the drawings of pre-
served material made by one who had seen, and possibly sketched in color, the material in
the living condition. That all the drawings were not made by the same person seems
obvious. Whatever their origin, all who have seen them agree that most of them are
remarkably well done.
WRITTEN RECORDS LEFT BY BASHFORD DEAN
Dean’s notes concerning Heterodontus comprise three documents: First, a notebook
containing a list of embryos collected (see also page 654), a very few miscellaneous notes,
and a large number of rough sketches of embryos. Some of these sketches are in color, and
are presumably made from living embryos as a preliminary to more finished portraits of
preserved material. Most of these drawings are on pieces of stiff cardboard adhering to
the pages of the notebook. Second, there is a notebook from which a considerable number
of pages have been cut out and are missing. Of the remaining pages, all are blank except
six, and these contain notes relating to the literature of paleontology and comparative
anatomy, with special reference to the phylogenetic relationships of Heterodontus.
Finally, there is a brief and very incomplete typed manuscript entitled: ‘‘Cestraciont
Sharks and their Development.” The “Table of Contents” attached to this manuscript
reveals that a very comprehensive article, paleontologic, phylogenetic, embryologic and
ecologic, was planned. Of this we find, in Dean’s manuscript, only an introduction,
brief sections dealing with the habits of the fish, methods of collecting its eggs, rate of
embryonic development, the egg and its capsule; and a final longer section on “Segmen-
tation” or cleavage. Of the 32 pages of this manuscript, 9 are devoted to cleavage. The
text here is almost identical with portions of Dean’s article entitled “Reminiscence of
Holoblastic Cleavage in the Egg of the Shark, Heterodontus (Cestracion) japonicus Mac-
leay,” published in 1901. There is intrinsic evidence that the manuscript under con-
sideration was written at a considerably later date, for in it reference is made to Goodrich’s
The Embryology of Heterodontus japonicus 657
volume on ‘“‘Cyclostomes and Fishes” published in 1909. Therefore it appears that the
portion of Dean’s manuscript dealing with the phylogenetic aspects of cleavage is in-
tended as a repetition, with revision, of the contents of his article published in 1901.
Considering these written records in their totality, none of the miscellaneous notes
and only certain portions of the manuscript are in a condition suitable for publication
without revision. These portions will be quoted verbatim. The manuscript was
originally typed, but much of it is so complicated by changes and additions (in script)
that both its style and its organization are impaired. It seems best to treat these
portions as notes, to be rewritten and incorporated in the present article. Notwith-
standing its limitations, Dean’s manuscript does give us much interesting information
not recorded elsewhere.
In concluding the introductory portion of his manuscript, Dean made the following
acknowledgments:
Before beginning his descriptive paper, the writer wishes to acknowledge numerous
courtesies which were extended him during various stages of his work. Especially to his
colleagues in Japan, Dean Mitsukuri and Professor Ijima his sincere thanks are due for ar-
rangements made at Misaki which resulted in the success of his collecting. He acknowledges
also his indebtedness to the assistant at the station, Mr. T. Tsuchida, whose never-failing
patience and diplomacy stood in good stead with the fisherpeople. Finally, he is indebted
to Dr. Naohide Yatsu, whose help, at all seasons and in all ways both in Misaki and in New
York, greatly lightened the burden of the work.
CLASSIFICATION AND SYNONYMY
Regan (1908) grouped the species of living Cestraciontidae (Heterodontidae) into
two genera, Gyropleurodus and Cestracion. Nearly all later authors recognize only one
genus (variously designated Heterodontus, Cestracion or Centracion) of the living Hetero-
dontidae. The species included in this genus are collectively equivalent to those of
Regan’s two genera. The common name Bullhead Sharks has been used by Jordan and
Evermann (1896), by Bridge (1904), and by many later authors, for the members of the
family Heterodontidae.
HETERODONTUS AND HETERODONTIDAE
In the present article I have adopted the generic name Heterodontus for the six
species of Bullhead Sharks represented by specimens living at the present time. Of these,
the best-known is the Port Jackson Shark, H. phillipi (Text-figure 4). For the genus
a synonym, Cestracion, is so firmly imbedded in the literature that it cannot be ignored.
Nevertheless, there are fairly convincing reasons why the name Heterodontus should
prevail. For my information regarding this matter I am indebted chiefly to Dumeéril
(1865, pp. 423-426); Maclay and Macleay, (1879, pp. 303 and 309) and Garman (1913,
pp. 4, 155, and 180).
658 Bashford Dean Memorial Volume
Text-figure 4.
A full-grown female Port Jackson Shark, Heterodontus phillipi, photographed from life. The four posterior
gill-slits, which were indistinct in the original, have been strengthened.
After Saville-Kent, 1897, p. 194.
SYNONYMY
The term Heterodontus has priority over Cestracion, having been used by Blainville
in 1816. The word means literally “different teeth”, thus describing one of the most
striking characteristics of the genus (Text-figure 10, page 670). The word Cestracion was
first used by Klein, in 1742 and again in 1776, as a name for the Hammerhead Sharks, and
has since been used by Duméril to designate the group of sharks termed, by Cuvier,
Zygaena. In 1817 Cuvier, without assigning any reason, gave the generic name Cestracion
to the Port Jackson Shark, the only living species of Bullhead Shark known at that time.
Presumably he did not know that Blainville, a year previously, had already given to that
species the generic name Heterodontus. Concerning the precise meaning of the name
Cestracion (from the Greek) there seems to be room for doubt. The matter is discussed
by Maclay and Macleay (1879) and by Garman (1913).
The generic name Centracion was given to one of the Bullhead Sharks by Gray (1831)
in the first number of his ““Zoological Miscellany” (p. 5). There he described a new species
named by him Centracion zebra. Gray did not explain his choice of the word Centracion,
and possibly the spelling was a mistake, for he wrote Cestracion instead of his own
term Centracion when, in 1851, he adopted the name Heterodontus for the genus.
Garman (1913) followed Klein and also Duméril in adopting Cestracion as the generic
name for the Hammerhead Sharks. In his choice of the name Centracion for the Bullhead
Sharks, Garman was not so fortunate. He objected to the name Heterodontus for the
reason that the word Heterodon, identical in derivation, had been applied by Latreille
(1802) to a group of reptiles. To the present writer this objection does not seem so
serious as the possibility that Centracion might be mistaken for Cestracion when these
The Embryology of Heterodontus japonicus 659
names are used for different genera of sharks. I have not found the name Centracion used
by any writers other than Gray and Garman.
For the reasons stated, I prefer the generic name Heterodontus Blainville for those
species of Bullhead Sharks that are represented by specimens living at the present time.
Since many authors, mainly paleontologists, have used the name Cestracion for the same
genus, it is necessary to recognize this term in reviewing their publications. For con-
venient reference, I have compiled the following synonymy:
HETERODONTUS (Blainville)
Port Jackson Shark (in genus Squalus). Phillip, 1789, Voyage to Botany Bay, pp. 283-284, pl.
Heterodontus. Blainville, 1816, Bull. Soc. Philom. Paris, 3. ser. 3, p. 121 (not Heterodon
Latreille, 1802).
Les Cestracions. Cuvier, 1817, Régné Animal, II, p. 129 (not Cestracion Klein, 1742 and
1776; nor Walbaum, 1792).
Centracion. Gray, 1831, Zool. Misc., I, p. 5.
Heterodontus, Tropidodus, and Gyropleurodus. Gill, 1863, Proc. Acad. Nat. Sci. Philadelphia,
14, p. 489.
Heterodontus. Duméril, 1865, Histoire Naturelle des Poissons, I, p. 424.
Heterodontus Bl. Maclay and Macleay, 1879, Plagiostomata of the Pacific. Proc. Linn. Soc.
New South Wales, 3, p. 309.
Heterodontus Bl. Ogilby, 1890, Australian Palaeichthyes. Proc. Linn. Soc. New South Wales,
2. ser. 4, p. 184.
Cestracion Cuvier. Woodward, 1889, Catalogue Fossil Fishes British Museum. Part I,
p- 331. Woodward, 1891, Hybodont and Cestraciont Sharks of the Cretaceous Period.
Proc. Yorkshire Geol. and Polytech. Soc., 12, part 1, p. 67.
Heterodontus Bl. Jordan and Fowler, 1903, Proc. U.S. Nat. Mus., 26, p. 599.
Centracion. Garman, 1913, Plagiostomia. Mem. Mus. Comp. Zool., 36, p. 180.
Having adopted the name Heterodontus for the genus that includes the only living
representatives of the Bullhead Sharks, I think it appropriate that the family name for
these sharks should be Heterodontidae. This name or its equivalent in a different language
has already been used, in the sense indicated, by several authors: e.g., Striiver, 1864;
Dumeéril, 1865, p. 623; Maclay and Macleay, 1879, p. 307; McCoy, 1890; Ogilby, 1890,
p. 184; Bridge, 1904 (“Cambridge Natural History”’, vol. VII, p. 444); Jordan and Clark,
1930, p. 10. Since Klein (1742), Duméril (1865), and Garman (1913) have assigned the
generic name Cestracion to the Hammerhead Sharks, it seems advisable to reserve
the name Cestraciontidae for the family that includes these sharks, as done by Garman
(1913, p. 155). Nevertheless, it should be borne in mind that the name Cestraciontidae
has been widely used, particularly by paleontologists, for the family that includes the
genus Heterodontus (Cestracion). It is so used by Woodward, 1889 (“Catalogue Fossil
Fishes British Museum,” Part I); Regan (1906 and 1908); and Zittel (1911, 1923 and 1932).
These are authors who retain the name Cestracion for the genus of Bullhead Sharks under
consideration. Goodrich (1909) uses the name Cestraciontidae for the family though he
seems to prefer Heterodontus for the genus.
660 Bashford Dean Memorial Volume
COMMON NAMES—BULLHEAD SHARKS
In view of the existing confusion in the use of scientific names for the genus and
family under consideration, the need for an undisputed common name is obvious. A few
authors (Waite, 1896; Dean, 1901.2 and 1904; and Whitley, 1938 and 1940) have used the
term Port Jackson Shark in a generic sense; but to the present writer this practice seems
very objectionable. For more than a century, the name Port Jackson Shark had been used
for one species only—the one first found at Port Jackson—save in a few instances where
the identification of species was incorrect.
Waite (1898 and 1899) has referred to Heterodontus galeatus, in which the supraor-
bital ridges are very tall, as the “Crested Shark”, and Whitley (1938 and 1940) has called
it the “Crested Port Jackson Shark”. The name Crested Shark would be appropriate for
the entire genus, but it has not been so used. Whether it would apply to the entire
family Heterodontidae (Cestraciontidae) as at present constituted (following the most
recent classification, that of Zittel, 1932) is problematical.
BULLHEAD SHaRKs.—There is no satisfactory common name that has been
used exclusively to designate all species of the genus Heterodontus, but the term Bullhead
Sharks (from the form of the head and snout) has been used by Jordan and Evermann
(1896) and by Bridge (1904) for the family Heterodontidae. Since all the surviving species
of this family belong to one genus, Heterodontus, the name Bullhead Sharks will serve the
needs of those who are mainly interested in recent forms. The same consideration applies
even though many genera (e.g., Hybodus) included by Bridge in the family Heterodontidae,
are now assigned toa separate family, the Hybodontidae. The fact that the common name
Bullhead Shark seemingly applies to two (closely related) families of sharks, one entirely
extinct, need trouble no one—least of all the paleontologists, who are not much interested
in common names.
The name Bullhead Shark is appropriate for all six species of Heterodontus. Fremin-
ville’s drawing (1840) of H. quoyi, which shows a small head, is inaccurate. A better
drawing of the same specimen, by Valenciennes (1846), is reproduced as my Text-figure
16, page 676. For related fossil forms, the evidence is naturally incomplete; but an
example with nearly perfect skeleton may be found in Hybodus hauffianus E. Fraas (Text-
figures 27 and 28, page 695). The profile of the head and anterior part of the body
bears a marked resemblance to Heterodontus as represented by my specimens of H. quoyi
and H. francisci, described in a later section of this article. These specimens (two of each
species) are not only “bullheaded” but more or less humpbacked, like the fossil Hybodus,
in the region dorsal to the bases of the pectoral fins. This feature is not represented in
some drawings of Heterodontus; but it is shown in Garman’s outline drawing of an adult
H. phillipi (1888, Fig. 1, pl. 18); in Maclay and Macleay’s drawings of a very young
specimen of H. phillipi (my Text-figure 8, page 668) and of a young female H. japonicus
(my Text-figure 23, page 691); in Jordan’s portrayal (1905, Fig. 315) of an adult H.
francisci; also in Kumada and Hiyama’s figure (1937) of an adult Gyropleurodus peruanus
(Heterodontus quoyi). Dean’s photograph of a fresh-caught Japanese Bullhead Shark (my
The Embryology of Heterodontus japonicus 661
Text-figure 3) shows no more than a faint suggestion of this humpbacked appearance. The
hump is only slightly developed in the adult Heterodontus phillipi photographed (from
life) by Saville-Kent (my Text-figure 4). In one of my specimens of H. francisci, the hump
is so low as to be scarcely noticeable. On the basis of all the available data, one can scarce-
ly say that the hump is typical for the genus Heterodontus. It occurs in at least four
species, but is decidedly variable. In those individuals in which the hump is well de-
veloped, the head and “shoulders” have a profile mildly suggestive of a buffalo bull. This
resemblance may be partly responsible for the name “Bullhead Shark.”
FAMILY AND GENERIC CHARACTERS
In this section we are concerned with the distinctive characters common to those
representatives of the family Heterodontidae that have survived to the present time.
Since all recent species belong to one genus, Heterodontus, the distinction between family
and generic characters is, for our purpose, of little importance. In the family Hetero-
dontidae, Bridge (1904) includes at least five other genera that are known only as fossils;
nevertheless, his brief description constitutes an excellent introduction to the study of
living Heterodontids. Some points in the following quotation (from Bridge, 1904, p. 444)
are illustrated by references, in square brackets, to figures in the present article.
Family Heterodontidae (Bullhead Sharks)
Head large and high, with a blunt snout projecting but little in front of the small and
almost terminal mouth, and with prominent supraorbital crests [Text-figures 3, 4 and 5]. Trunk
thickset and almost trihedral, covered with fine shagreen. Nostrils ventral but nearly termi-
nal, with oronasal grooves [Text-figures 25and 40, pages 692 and 711]. Spiracles small, beneath
the eyes [Text-figures 3 and 4]. Two dorsal fins, each with a spine in front, the first opposite
the interval between the pectorals and the pelvics, the second in front of the anal. Vertebral
centra asterospondylic when fully developed. Palatoquadrate cartilages with an extensive
articulation with the sides of the preorbital regions of the cranium [Text-figure 33, page 700],
the normal suspensoria of a hyostylic skull (hyomandibular cartilages) taking little share in
their support. Dentition similar in both jaws [Text-figures 11 and 14c, pages 671 and 673].
Teeth at the symphysis numerous, small and conical, furnished with three to five cusps in the
young; those behind broad and padlike, arranged in oblique rows, the teeth forming the two
middle rows being much larger than those in the front or behind. Living species, oviparous.
Egg cases large with an external spiral lamina [Text-figure 37, page 706; and Figures 76 to
78, plate VII].
Continuing, Bridge notes that all the living representatives of this family are in-
habitants of the Pacific Ocean, and that they feed principally on molluscs, the shells of
which are crushed by their massive grinding teeth. According to Bridge, the different
species vary in size (length) from two to five feet.
Some additional characters of the family Heterodontidae (Cestraciontidae) are listed
by Goodrich (1909) as follows: The base of the pectoral fin grows forward below the
last three branchial slits (my Text-figure 6, page 666). The pectoral girdle is very powerful
(see also Daniel, 1915, Fig. 6, pl. III). According to Goodrich the suspension of the
662 Bashford Dean Memorial Volume
jaws of Heterodontus is hyostylic, but with a very extensive articulation of the palato-
quadrate with the cranium, so that the hyomandibular scarcely acts as a real support
(my Text-figure 33, page 700). The suspension of the jaws is further discussed on pages
699 to 701 of the present article.
Garman’s definition (1913) of the family Heterodontidae (his Centraciontidae)
attempts to separate family characters from generic ones; but since he excludes fossils, the
description really applies to only one genus, Heterodontus. Garman writes:
The living species of this family are small sharks which have short bodies and heads,
blunt snouts, small spiracles below the hinder part of the eye, a narrow mouth near the end of
the snout, with about four lobes in each half of the upper lip, both cuspidate teeth and grind-
ers, five gillopenings of which several are above the pectorals, eyes without nictitating
membranes or folds, nostrils connected with the mouth by naso-oral grooves, without cirri, two
dorsals each preceded by a strong rigid spine, an anal behind the second dorsal, a short deep
caudal, small carinate scales, a preorbital articulation between upper jaw and skull, and
asterospondylous vertebrae.
In the phrase “eyes without nictitating membranes or folds”, it is not quite clear
what Garman means by the word “folds”. If he means a fold of ordinary skin, then my
adult specimen of H. quoyi is an exception, for it possesses a fold of skin capable of over-
lapping the eye somewhat like an upper eyelid.
The genus Heterodontus, which Garman calls Centracion, is characterized by him
(1913) as follows:
Head short, snout blunt, crown narrowed, between strong orbital ridges. Eyes small,
lateral. Nostrils with two thick valves reaching the mouth and curving toward the grooves.
No narial cirri. Mouth narrow, with thick labial folds on both jaws. Teeth alike in upper
and lower jaws, cuspidate in the anterior series, elongate longitudinally ridged grinders
posteriorly. Pectorals large, dorsals moderate, anal small, caudal short.
The present writer has not been able to examine specimens of all species of Hetero-
dontus, but the evidence at hand indicates that unusual breadth of the head and anterior
part of the body, and decided flatness of the ventral surfaces of both head and body, are
typical for adult specimens of this genus. A slightly humpbacked appearance, observed in
my specimens of H. quoyi and H. francisci, is possibly a generic or even a family character.
The supraorbital ridge leans outward, overhanging the eye. The anterior teeth are
quincuspid in the very young; and acutely tricuspid in older specimens, with the median
cusp increasingly predominant. In the adult they are often simple, becoming blunt
when old. The lips, nasal apertures and naso-oral grooves of a single specimen of Hetero-
dontus, probably francisci, have been described in detail by Allis (1919, pp. 158-164 and
Figs. 6 and 7, pl. I.
A vestigial sixth branchial arch was found by Hawkes (1905) in two species of
Heterodontus—phillipi and francisci. The other species were not available for exami-
nation. Hawkes states that the presence of a rudimentary sixth branchial arch in Hetero-
dontus is in harmony with the view that the Heterodontidae are in some respects inter-
The Embryology of Heterodontus japonicus 663
mediate between the Notidanidae and Chlamydoselachidae on the one hand, and the
remaining Selachii on the other. In Heterodontus francisci as figured by Daniel (1915)
the vertebral column is better developed, and the notochord is more constricted than
in Heptanchus and Chlamydoselachus. Presumably these structures are much alike in
all species of Heterodontus.
THE SPECIES OF HETERODONTUS
In Volume VIII of his “Catalogue of the Fishes in the British Museum”’, under the
heading Cestraciontidae, Giinther (1870) lists and briefly describes four species of Ces-
tracion (Heterodontus): phillipi, quoyi, francisci, and galeatus. Another species known at
that time, Heterodontus (Cestracion) zebra Gray, was lumped (by Gunther) with phillipi.
Thus it appears that, of the species now recognized, all but one (japonicus) were known at
this early date (1870), though zebra was not uniformly recognized as a distinct species.
As we shall see later, even japonicus was then represented in museum collections, and
drawings of this species had been published before it was identified as a species distinct
from phillipi.
Garman (1913, pp. 180-181) gives a key to the species of Heterodontus, which he
calls Centracion, based mainly on the position and shape of the anal fin, the position of
the first dorsal with respect to the pectorals, and the color pattern of the entire body.
This is followed by a synonymy and a comprehensive list of the distinctive external
characters for each species. Garman’s classification agrees, in the main, with that of
Maclay and Macleay (1879, 1884 and 1886) but differs from that of Regan (1908).
GARMAN’S KEY TO THE SPECIES OF CENTRACION (HETERODONTUS)
Base of anal about two-thirds of its length distant from the caudal.
Origin of first dorsal above the hind portion of the pectoral base, hind margin concave.
Bands transverse and broad to absent........................ galeatus [page 686]
Base of anal nearly one length distant from the caudal.
Origin of the first dorsal above the forward part of pectoral base, hind margin concave.
SpotsmblackssmallRiccattered enn een nina a eae aee francisci [page 681]
Base of anal two-thirds of its length distant from the caudal.
Origin of first dorsal behind the end of the pectoral base, hind margin convex.
Spots black, moderate, more or less grouped in twos and fours......... quoyi [page 676]
Base of anal fin two or more times its length from that of the caudal.
Origin of first dorsal above the middle of the base of the pectoral, hind margin deeply
concave.
Band sitransversessia ci Ow. ree elaine reaee zebra [page 675]
Base of anal little less than twice its length from that of the caudal.
Origin of first dorsal above mid-pectoral base; fin somewhat concave on hind margin.
Bands both transverse and longitudinal.......................phillipi [page 664]
Base of anal about one and one-fourth times its length from that of the caudal.
Origin of first dorsal above the end of the pectoral base, hind margin concave ([some-
times] convex in second dorsal).
Bandsitransyerse broad pape eer tee ie ae eee eran: japonicus [page 688]
664 Bashford Dean Memorial Volume
According to Garman there are six species of Heterodontus (Centracion) living at the
present time, and these are found only in the Pacific Ocean. But it is not certain that
sharks of the genus Heterodontus originated in the Pacific, since fossil Heterodonts have
been found in Bavaria and in England (see p. 698).
Two species are confined to the eastern Pacific Ocean: Heterodontus francisci off the
coast of California and the western coast of Mexico; and H. quoyi around the Galapagos
Islands (it has also been taken at the Lobos de Fuero Island, nearer the coast of Peru). In
the western Pacific, H. phillipi, the Port Jackson shark, is found off the coasts of eastern
and southern Australia, and off New Zealand; and H. galeatus occurs off New South
Wales and Queensland. The two other species are H. zebra, ranging from China (rarely
from Japan).to the East Indies; and H. japonicus from the coasts of the Japanese islands
south of Hokkaido. Thus two species occur in Japanese waters: H. zebra has been
taken in the Sagami Sea, but the species usually found there is H. japonicus, the Japanese
Bullhead Shark.
It is not necessary here to go into details concerning the surface anatomy of the
adults of these species, but a brief account of their distinctive characters will be helpful.
The species are here discussed in the order of their recorded discovery —meaning not
merely the capture and description of a specimen but its correct identification. In the
section devoted to each species, jaws and teeth are described last.
HETERODONTUS PHILLIPI BLAINVILLE
This, the Port Jackson Shark, is the best-known species, and for half a century it was
the only species recognized. According to Whitley (1940) it occurs in the following
Australian waters: South Queensland, New South Wales, Victoria, South Australia,
Great Australian Bight to Southwestern Australia; commonest in the south. Found in
littoral waters to depth of 94 fathoms.
The specific name, phillipi, has been spelled in different ways, but the species was
named for Governor Phillip. His name is thus spelled on the title page of the book
describing his voyage to New South Wales, with observations on the fauna and flora of
that region. This book (Phillip, 1789) contains the first authentic description and draw-
ings of the Port Jackson Shark—so named by Phillip because his specimen was captured at
Port Jackson (Sydney Harbor), Australia. It was called Le Squale Phillip by Lacépede
(1798); Heterodontus phillipi by Blainville (1816); and Cestracion phillipi by Cuvier (1817).
An extensive synonymy is given by Garman (1913) under the title Centracion phillipi.
According to Maclay and Macleay (1879) this shark was called Tabbigaw by the
Sydney aborigines. McCoy (1890) wrote that because of the form of the head and muzzle
it was called the Bulldog Shark by Victorians. SavilleKent (1897) states that Oyster-
crusher, Pigfish, and Bulldog Shark are names by which the Port Jackson Shark was known
locally to Australian fishermen.
Mainly because of its historical importance, the somewhat conventionalized (but
otherwise correct) drawing of the Port Jackson shark in the volume describing Phillip’s
The Embryology of Heterodontus japonicus 665
Text-figure 5.
A Port Jackson Shark, Heterodontus phillipi Blainville. This female specimen, 610 mm. (24 inches) long,
was captured at Port Jackson (Sydney Harbor), Australia.
After Phillip, 1789, pl. facing p. 283.
voyage is reproduced here (in Text-figure 5). For nearly a century this drawing remained
the best portrait of Heterodontus phillipi. Under the heading “Port Jackson Shark”,
Phillip described the “new species” (in one sentence!) as follows:
The length of the specimen from which the drawing was taken is two feet; and it is
about five inches and an half over at the broadest part, from thence tapering to the tail: the
skin is rough, and the colour, in general, brown, palest on the under parts: over the eyes on
each side is a prominence, or long ridge, of about three inches, under the middle of which the
eyes are placed: the teeth are very numerous, there being at least ten or eleven rows; the
forward teeth are small and sharp, but as they are placed more backward, they become more
blunt and larger, and several rows are quite flat at top, forming a kind of bony palate, some-
what like that of the Wolf-fish; differing, however, in shape, being more inclined to square
than round, which they are in that fish: the under jaw is furnished much in the same manner as
the upper: the breathing holes are five in number, as is usual in the genus: on the back are two
fins, and before each stands a strong spine, much as in the Prickly Hound, or Dog Fish: it has
also two pectoral, and two ventral [pelvic] fins: but besides these, there is likewise an anal
fin, placed at a middle distance between the last and the tail: the tail itself, is as it were divided,
the upper part much longer than the under.
One may add that, in the words of Garman (1913), the spiracle is small, below the
orbit and immediately behind a vertical from its posterior edge. The distribution of
the lateral-line system of Heterodontus phillipi was earlier (1888) figured and described by
Garman. For characters diagnostic of the species, see Garman’s key. The photograph
by SavilleKent (my Text-figure 4) probably gives a better conception of the general
appearance of this shark than any drawings reproduced herein.
Lesson’s colored figure (1826) of a male Heterodontus (Cestracion) phillipi has been
666 Bashford Dean Memorial Volume
criticised by Maclay and Macleay (1879), who alleged that it is so unlike the fish it is
intended to represent as to suggest a doubt of its being the same species. In 1884 Maclay
and Macleay stated definitely that this figure, which they call “a very bad one”, does not
represent the Port Jackson Shark. In Lesson’s figure the color pattern of the body is
unlike that ofany other drawing of Heterodontus phillip: known to me, and the shape of the
ventral lobe of the caudal fin is unlike that shown in all other drawings of specimens
belonging to the genus Heterodontus. It is not necessary to reproduce this figure, since it
was evidently drawn from a dried and distorted specimen.
Miller and Henle’s full-length colored portrait (1841, pl. 31) labelled Cestracion
phillipi is reproduced, under its proper name, as my Text-‘figure 21, page 690. In 1879
Macleay expressed a doubt as to the identity of the species represented by this figure, and
in particular stated that the form of the six-cusped tooth pictured by Muller and Henle
(but omitted from my Text-figure 21) had never, they believed, been seen in any adult
specimen of the Port Jackson Shark. Further, in 1884, Maclay and Macleay stated that
Miller and Henle’s figure is most likely of the Japanese species, the number of vertical
bands being identical, and that the tooth portrayed in the same plate is certainly not of
either species. At the present time one can scarcely doubt that Muller and Henle’s
figure of the entire fish is a fairly accurate representation of the Japanese Bullhead
Shark, Heterodontus japonicus. The same may be said of Brevoort’s drawing (1856) of
a specimen collected by the Perry Expedition to Japan. This specimen was labelled
Cestracion phillippi; it is reproduced, under its proper name, as Text-figure 22, page 690.
Striiver (1864) has contributed what appears to be an accurate drawing of a badly
posed specimen of Heterodontus phillipi. Perhaps this fish had been hardened in a laterally
Text-figure 6.
A full-grown male specimen of the Port Jackson Shark, Heterodontus phillipi, 795 mm. (31.4 inches)
long. The external opening of the spiracle (retouched to make it more clearly visible) is shown behind,
and a little below, the eye.
After Maclay and Macleay, 1879, Fig. 8, pl. 23. Right and left are here reversed.
The Embryology of Heterodontus japonicus 667
Text-figure 7.
Dorsal view of the 795-mm. male specimen of Heterodontus phillipi shown, in lateral view, in Text-figure 6.
The external openings of the spiracles are shown in the dark band crossing the head.
After Maclay and Macleay, 1879, Fig. 3, pl. 22.
flexed condition. The color pattern is not shown. The external spiracular opening is
unusually large. It does not seem necessary to reproduce this figure.
In the order of historical sequence, the next authentic drawings of Heterodontus
phillipi that have come to my attention are those of Maclay and Macleay (1879). Text-
figure 6 is a copy of their drawing of an adult male specimen in lateral view. This is
probably the best drawing of an adult male Port Jackson shark ever published. One
should notice particularly the large head and the color pattern of the head and body.
The authors state that the skin is roughly shagreened, and that the color in the fresh
specimen is reddish-brown above and yellow with a pinkish tinge beneath. The color
pattern (made up of brownish-black stripes) becomes indistinct within a few hours after
death and in this drawing of a preserved specimen the color pattern is represented as seen
in perfectly fresh specimens. In addition, the authors portray a dorsal view of the same
adult specimen (my Text-figure 7). One is impressed by the breadth of the head including
the branchial region. The color pattern of the dorsal surface is decidedly more complex
than that of the lateral surface. The authors state that the average size of adult specimens
of the Port Jackson Shark of both sexes is a little over three feet and that they seldom, if
ever, attain a length of four feet. The external reproductive organs of an adult male are
represented by Maclay and Macleay (1879) in their Figs. 24 and 25, pl. 24. Each
myoxpterygium is armed with a sharp spine.
Of particular interest are Maclay and Macleay’s figures (1879) showing lateral and
dorsal views (my Text-figures 8 and 9) of a very young specimen only 225 mm. (8.8 inches)
long. The authors state that this specimen was probably hatched only a day or two previ-
668 Bashford Dean Memorial Volume
Text-figure 8.
Lateral view of a very young (recently hatched) female specimen of the Port Jackson Shark,
Heterodontus phillipi, about 225 mm. (8.8 inches) long, drawn while fresh.
After Maclay and Macleay, 1879, Fig. 5, pl. 23. Right and left are here reversed.
ously; but to me it seems likely that it was about two weeks old. The entire color
pattern is more distinct and somewhat more complex in this young specimen than in the
adults. Concerning this specimen Maclay and Macleay wrote: ‘The very remarkable
marking, the rounded form of the head and the proportionally large tail are peculiar to
this stage”. From the dorsal view of this specimen, we see that the head is not so broad,
proportionally, as in the adult.
McCoy (1890) contributed two figures, in color, representing side views of male and
female specimens of Heterodontus phillipi. The delicacy of the outlines of these drawings
makes them unsuitable for reproduction here. In these figures the color pattern is not
well shown, but McCoy’s detailed description of the distribution of the dark-brown
stripes corresponds closely with the pattern shown in Maclay’s drawings (lateral and
dorsal views). According to McCoy the dark-brown bands are most distinct in the
young, nearly obsolete in the old, and invisible in stuffed, dried, or spirit specimens.
The photograph of the Port Jackson Shark by Saville-Kent (1897) is reproduced as
my Text-figure 4, page 658. The specimen was alive when photographed. The original
figure measures six and one-half inches long and is said to be one-tenth natural size. This
would make the shark over five feet long. If the reduction is accurately stated, this is the
largest Port Jackson Shark on record; but experience shows that one cannot always depend
on records of this kind.
Waite (1898) collected specimens of the Port Jackson Shark, Heterodontus phillipi,
from 14 different stations, and records that none of the specimens was longer than two
feet. The majority were but little over 18 inches. He states that this shark is not known
to grow longer than four and one-half feet, and that it is harmless.
The Embryology of Heterodontus japonicus 669
Whitley’s excellent representation (1940, Fig. 52) of a female Heterodontus phillipi,
said to be after Waite, bears a remarkable resemblance to Saville-Kent’s photograph
reproduced as my Text-figure 4. The four posterior gill-slits and the color pattern of the
sides of the body are more distinct in Whitley’s figure. In addition, Whitley (1940, Fig.
53) has published an excellent original drawing of a female Heterodontus phillipi. Concern-
ing the coloration, he writes: “Color grayish to light brownish. A dark blotch on snout.
A blackish interorbital bar as broad as eye, continued and expanded below eye. A series
of blackish stripes on body rather like harness.”
Glands associated with the dorsal fin spines of certain sharks have been studied by
Evans (1924). In Squalus, this author found a large groove along the base of each dorsal
spine, on the side facing the fin. The groove is filled with a follicular gland, which was
studied microscopically. Evans cites evidence that the secretion discharged by this gland
has venomous properties. He states further that the dorsal fin spines of Cestracion
(Heterodontus) phillipi are similar to those of Squalus, but with a shallower groove. This
groove likewise contains a follicular gland, but the nature of the secretion was not studied
in Heterodontus. The author makes comparisons of the dorsal fin spines of Squalus and
Cestracion (Heterodontus) with those of some fossil Cestracionts, and of Hybodus. The
presence of a large groove along the bases of the dorsal fin spines of these fossil forms
suggests that, in life, glands were present at the bases of these spines also.
Text-figure 9.
Dorsal view of the very young female Port Jackson Shark, Heterodontus phillipi, about 225 mm. (8.8 inches)
long, shown in lateral view in Text-figure 8. The drawing was made while the specimen was fresh.
After Maclay and Macleay, 1879, Fig. 1, pl. 22.
670 Bashford Dean Memorial Volume
Jaws anp TeetH.—Goodrich (1909) contributes an outline drawing of an in
complete skull of Heterodontus phillipi, here reproduced as Text-figure 33, page 700.
This drawing is introduced primarily to show the mode of suspension of the jaws; but
when we compare this figure, showing these jaws in lateral aspect, with other figures
(Text-figures 10, 11 and 14) showing them in dorsal and ventral aspects, we are impressed
by their massive pincer-like character—somewhat like the jaws of Heptanchus outlined by
Text-figure 10.
Teeth of the Port Jackson Shark, Heterodontus phillipi. Whether the figure
represents an upper or lower jaw is not stated, but apparently it is a lower jaw.
After Phillip, 1789, pl. facing p. 283.
Goodrich, 1909, Fig. 59a. One can readily imagine how powerful these jaws are
when equipped with the grinding teeth—set well back toward the angle of the jaws—and
with the musculature necessary for crushing the shells of molluscs that form the principal
food of this species of Heterodontus. Garman also (1913, Atlas, Fig. 4, pl. 47) has figured
the jaws of Heterodontus phillipi in lateral view, but in form so different from Goodrich’s
portrayal that one might think the two drawings were made from different species.
Phillip’s drawing (1789) of the teeth of the Port Jackson Shark is reproduced here as
Text-‘figure 10. The author does not state whether this is an upper or a lower jaw, but
upon comparison with the figures of Striiver (1864), Maclay and Macleay (my Text-figure
11) and McCoy (my Text-figure 14) it appears to be a lower jaw. In this specimen
The Embryology of Heterodontus japonicus 671
(Text-figure 10) there are 33 rows of teeth. The anterior teeth (13 series or transverse
rows) are distinctly tuberculate, but, due to the overlapping of the teeth in each row,
their form is not completely shown except in the most anterior members of each series.
Each anterior tooth possesses one large central cusp, and there may occasionally be seen
in the drawing a rudimentary lateral cusp on one or both sides of the central cusp. The
posterior teeth (ten rows on each side) are
large, smoothly rounded, and in their natural
arrangement combine to form an exposed
surface resembling that of a stone-block pave-
ment. Thus the anterior teeth are adapted for
holding the prey, the posterior ones for crush-
ing and grinding it.
Striiver (1864) made drawings of the teeth
of both upper and lower jaws of Heterodontus
phillipi. With respect to the dentition, upper
and lower jaws are much alike, save that the
lower is slightly shorter and more obtuse in
front, which makes some difference in the
arrangement of the teeth. In this respect the
lower jaw resembles the jaw figured by Phillip
(1789); but in Striiver’s figures both jaws show
a more gradual transition between anterior
(cusped) teeth and posterior (grinding) teeth,
so that the line of demarcation between the
two kinds of teeth is not sharply defined.
However, one might assign 15 transverse rows
to the anterior region in the upper jaw, and 13
rows to this region in the lower jaw. The total
number of teeth in the upper jaw is 33, in the
lower jaw 31. In Striiver’s figures the anterior
teeth are pointed but without obvious second-
ary cusps; each posterior tooth has an indistinct
longitudinal ridge.
Miklouho-Maclay (in Maclay and Macleay,
1879) figured the teeth of upper and lower jaws
in both adult and young specimens of H.
phillipi. The dentition of an adult, as shown in
his figures (my Text-figure 11) resembles that
represented in Striiver’s drawings (1864). As
in Struver’s figure, the lower jaw is shorter
than the upper, and is more obtuse in front.
Text-figure 11.
Teeth of an adult Heterodontus phillipi:
A, upper jaw; B, lower jaw.
After Maclay and Macleay, 1879, Figs. 16 and 17, pl. 24.
672 Bashford Dean Memorial Volume
The transition between anterior (cusped) teeth and posterior (grinding) teeth is so
gradual that any division into two types must be somewhat arbitrary. However, of
the 33 rows of teeth on the upper jaw one might assign 19 rows to the anterior region,
leaving 14 (seven on each side) in the posterior region. In the lower jaw there are 32
rows of teeth of which 14 rows may be
assigned to the anterior region, leaving
18 (nine on each side) for the posterior
region. Thus there seem to be more rows
Text-figure 12.
Anterior teeth of a young Hetero-
dontus phillipi about 761 mm. (22.1
inches) long: A, from the upper;
B, from the lower jaw.
After Maclay and Macleay, 1879, Figs. 18a
and 18s, p. 24.
Text-figure 13.
of anterior (cusped) teeth om the upper Dentition of a very young (recently hatched)
jaw than on the lower (as in Struver’s female Heterodontus phillipi about 225 mm.
figure). In another specimen Maclay (8.8 inches) long: A, upper jaw; B, lower jaw.
counted 34 rows of teeth on the upper After Maclay and Macleay, 1879, Figs. 14 and 15, pl. 24.
jaw and 31 on the lower. The largest
number of rows of teeth noted by Maclay was 36 on an upper jaw; the largest number
on a lower jaw is not stated, but we infer that it was less.
In Maclay’s figures, as in Struver’s, the anterior teeth of the adult have only one cusp
each; but in Maclay’s figure these are more blunt as if worn by use. Maclay states that
The Embryology of Heterodontus japonicus 673
the anterior teeth (my Text-figure 12) of a not fully developed Heterodontus phillipi
761 mm. (22.1 inches) long are distinctly tricuspidate, the central cusp predominating,
while those of the adult become almost pavement-like, with an inconspicuous cusp. He
further states that on the posterior teeth of a young specimen 418 mm. (16.4 inches) long,
a longitudinal ridge is much more pronounced than in older specimens.
Maclay (Maclay and Macleay, 1879) portrayed also the dentition of both upper and
lower jaws in their very young specimen of Heterodontus phillipi only 225 mm. (8.8 inches)
long. Comparatively few teeth are exposed (my Text-figure 13) and these are nearly all
cuspidate. About 40 teeth are visible on the upper jaw and about 32 on the lower jaw,
roughly arranged in transverse rows of two or three teeth each, giving about 17 rows on
the upper jaw and 13 on the lower jaw. Most of these teeth have three to five cusps, and
seldom a predominating central cusp. The cusps are best developed in the most anterior
teeth and are less conspicuous posteriorly. They are absent in one or two teeth of
the last row on each side. Maclay states that some other teeth came into view after the
mucous membrane had been dissected off. He calls attention to “‘the very great similarity”
between the dental armature of the young Heterodontus and that of (adult?) Notidanids.
Text-figure 14.
Head and teeth of the Port Jackson Shark, Heterodontus phillipi, in three aspects: A,
anterior view of the head, mouth closed, showing exposure of teeth above and below.
B, teeth of lower jaw in natural size. C, mouth widely opened, to show the similarity
of dentition above and below.
After McCoy, 1890, pl. 113.
674 Bashford Dean Memorial Volume
McCoy’s descriptions and drawings (1890) of the teeth of H. phillipi (my Text-figure
14) are excellent. “Teeth alike in both jaws, the median front rows very small, acutely
tricuspid when young, simple and with obtusely triangular cusp in middle age, blunt and
hexagonal when old; more posterior teeth large, oblong, longer than broad, flattened,
arranged in oblique, spiral rows on each side of the jaw, the anterior and posterior ones
smaller than those in the middle.” His figure of the lower jaw (my Text-figure 14s)
reveals a distinct longitudinal ridge on each of the posterior grinding teeth—a feature
mentioned but not figured by Maclay (1879). The lower jaw shows a distinct line of
demarcation between anterior cusped teeth and posterior grinding teeth—as in the
figure by Phillip (Text-figure 10) but not to the same degree. In this jaw there are only
eleven transverse rows of anterior cusped teeth. These, with eight rows, on each side, of
posterior grinding teeth, make a total of 27 rows in this lower jaw. Textfigures 14a
and 14c show, respectively, the appearance of the mouth when it is closed and when it is
open. The lower jaw in Text-figure 14c is identical with that in Text-figure 148. The
upper jaw, shown in Text-figure 14c, likewise has 27 rows of teeth. Of these, 12 or 13
rows are anterior or cuspidate teeth. The transition between cuspidate and grinding
teeth is not so abrupt as it is in the lower jaw.
Garman (1913, Figs. 4 to 6, pl. 47) portrays the teeth of a male Heterodontus phillipi
about 864 mm. (34 inches) long. The transition between anterior (cuspidate) and posterior
(grinding) teeth is not so abrupt, in this specimen, as in some others. The dividing lines
here chosen are somewhat arbitrary. The upper jaw has 13 transverse rows of anterior
(cuspidate) teeth and 10 rows (5 on each side) of posterior (grinding) teeth, making a total
of 23 rows. The lower jaw has 11 rows of anterior (cuspidate) teeth and 8 rows (4 on
each side) of posterior (grinding) teeth, making a total of only 19 rows. Garman’s figures
of the posterior grinding teeth or “molars” show on each tooth a distinct longitudinal
ridge or “keel”, and on each side of this, many fine transverse ridges. Garman states that
the ridges on the molars of younger specimens become less conspicuous with age and use,
and that the harder the food in a particular locality the fainter the ridges appear.
To summarize the recorded data on the dentition of the adult or nearly adult Hetero-
dontus phillipi, one may state that all the descriptions and drawings emphasize the decided
differences between anterior and posterior teeth—differences that suggested the generic
name, Heterodontus. When we compare the dentition of upper and lower jaws, we find
that Bridge’s statement “dentition similar on both jaws” is true of all specimens that have
been described. One may be more definite and explain that the dentition (meaning the
kind, number and arrangement of the teeth) is alike on upper and lower jaws, with certain
slight reservations. First, as McCoy states, there are usually ‘‘a few more rows in upper
than [in] lower jaw”. Using the meager data available we find that the average number of
transverse rows on the upper jaw (6 cases, average 31.0 rows) is slightly greater than
on the lower jaw (6 cases, average 28.8 rows). In only one instance (McCoy’s drawing) is
the number of rows of teeth the same on both jaws. The largest number of teeth recorded
The Embryology of Heterodontus japonicus 675
for an upper jaw is 36; for a lower jaw, 33. Second, I have noted that, in the figures of
various authors, there is a slight difference in the shape of the opposed surfaces of upper
and lower jaws: in the lower jaw this surface is a trifle shorter. This may account for the
difference in the number of rows of teeth. Third, in every case recorded the upper jaw
has more rows of anterior (cuspidate) teeth than the lower jaw.
HETERODONTUS ZEBRA GRAY
This species ranges from the coasts of China and (rarely) Japan, to the East Indies.
It was first described in 1831 by Gray, who named it Centracion zebra. In 1851 he adopted
the name Heterodontus for the genus.
The earliest drawings of this species that I have been able to find are those of
Maclay and Macleay (1886). These were made from a preserved specimen, a young
female about 518 mm. (20.4 inches) long, captured at Swatow in the South China Sea.
Text-figure 15.
A male specimen of Heterodontus zebra Gray, about 1220 mm. (48 inches) long.
From a drawing in color by Ito, 1931, Fig. 6, pl. V.
The color pattern is more adequately shown in my Text-figure 15, from a folio volume
entitled “Illustrations of Japanese Aquatic Plants and Animals”, published by the
Japanese Fisheries Society in 1931. This represents an adult male about 1220 mm. (48
inches) long. The Japanese common name is said to be “‘Simanekozame”’.
The most conspicuous peculiarity of this species is the presence of numerous narrow
transverse dark-brown stripes (Text-figure 15) which suggested the specific name, zebra.
Except in a few places, these dark-brown stripes alternate with lighter-brown narrower
ones. Garman (1913) states that in a 19-inch female specimen studied by him, the body
and head are more slender, the head more pointed and the fins longer, than in other species
of the genus. Maclay and Macleay’s drawing of a dorsal view of their specimen shows
head and body very narrow as compared with other species. In this drawing the head is
rotated slightly, so the width cannot be measured for comparison with the total length.
Maclay and Macleay’s figures show prominent supraorbital ridges in both lateral and
676 Bashford Dean Memorial Volume
anterior views but these are lacking in the Japanese drawing reproduced as my Text-figure
15. Maclay and Macleay state that the dorsal fins are very falcate. This feature is per-
haps exaggerated in their drawing, which was made from a preserved specimen; it is
more moderate and more life-like in the Japanese drawing. In the latter figure the
anterior margin of the pectoral fin is opposite the fourth gill-slit, while in Maclay and
Macleay’s figure it is opposite the second.
Tue TretH—According to Maclay and Macleay (1886), the anterior teeth of
their young female specimen of H. zebra (518 mm. long) were five-cusped. Garman (1913)
states that the anterior teeth are quincuspid in the young, tricuspid in the adult.
HETERODONTUS QUOYI FREMINVILLE
Examples of this species (Text-figure 16) have been taken off the western coast of
South America, specifically at the Galapagos and Lobos de Afuera Islands—the latter
Text-figure 16.
Heterodontus quoyi Freminville: a male specimen about 475 mm. (18.7 inches) long, taken at the Galapagos
Islands. The original figure, in color, is labelled Cestracion pantherinus.
After Valenciennes, 1846, Atlas (Poissons), Fig. 2, pl. 10.
close to the coast of Peru. In addition, a Heterodontid shark taken at the Lobos de
Tierra Island, Peru, belongs to this species. This specimen was described and figured by
Evermann and Radcliffe (1917) who named it Gyropleurodus peruanus. Of this fish they
write: “The species appears to be most closely related to the poorly described G. quoyi,
but differs in coloration, in insertion of anal, and relative size of pectoral”. After a careful
study of the matter, Beebe and Tee-Van (1941) conclude that all the Heterodontid sharks
thus far taken off the western coast of South America belong to the species peruanus
(quoyi) as redescribed by Valenciennes and later authors. They state that the alleged
differences between quoyi and peruanus do not exist, although there is some individual
variation in the color patterns. With this conclusion the present writer is thoroughly in
accord. The native name of H. quoyi is “Gato” (Nichols and Murphy, 1922).
The Embryology of Heterodontus japonicus 677
There remains some doubt concerning the identity of a Heterodontid shark taken off
the western coast of Mexico, or perhaps of Central America, which was described and
figured by Kumada and Hiyama (1937). They named it Gyropleurodus peruanus. Their
drawing portrays a shark in most respects like H. quoyi, but the color pattern is inter-
mediate between H. quoyi and H. francisci. Since the color pattern of the former is
somewhat variable, the drawing was probably made from a specimen of H. quoyi; but
there is no other record of the occurrence of this species so far north.
Heterodontus quoyi was first figured and described by Freminville (1840); and later
by Valenciennes (1846 and 1855). Their figures are based on the same specimen, a male
taken at the Galapagos Islands; but these differ so much that they might be considered
as representing two different species. Valenciennes called this specimen Cestracion
pantherinus, though it had been previously named Cestracion quoyi by Freminville. The
brief accounts by Duméeril (1865), Gunther (1870), Maclay and Macleay (1879) are based
on either Freminville’s or Valenciennes’ description and figure; they contain nothing
new. Maclay and Macleay’s figure (1879) is a copy of Freminville’s. Until Garman
(1913) described at least one new specimen (a female taken at the Galapagos Islands),
Freminville’s male specimen of H. quoyi remained the only example of the species. In
his very inadequate description, some comparisons with Heterodontus phillipi are
irrelevant since they involve the acceptance of erroneous features in Lesson’s (1826)
drawing of the Port Jackson Shark. Freminville’s figure of H. quoyi does not inspire
confidence, and I have therefore reproduced Valenciennes’ life-like portrait of the same
specimen (my Text-figure 16) as the basis of this account.
The length of Freminville’s specimen is variously recorded as a little more than
a foot and a half, by Freminville; 475 mm. (18.7 inches) by Valenciennes; 460 mm. (18.1
inches) by Dumeril; and two feet (evidently a blunder) by Maclay and Macleay. Gar-
man’s female specimen measured 18 inches long. Garman states that its body is rather
stout as compared with a specimen of H. zebra of equal length. Some passages in Garman’s
characterization imply that he had more than one specimen, but he does not give the
lengths of any others.
The most noteworthy feature of Freminville’s drawing of H. quoyi is the small size
of the head. The author states that the head is smaller and a little more elongate than
that of Cestracion phillipi. As portrayed by Freminville, the head is very small and
pointed. In Valenciennes’ drawing (my Text-figure 16) the head is proportionally much
larger. Garman does not say that the head of his specimen (or specimens?) is small. He
does write that the snout is blunt, the cheeks swollen, the eye and spiracle small. Fremin-
ville states that the supraorbital ridge is comparatively weak (“moins forte”) but Garman
records that it is strong, somewhat overhanging the orbit, not ending abruptly as in H.
francisci. In Valenciennes’ figure (my Text-figure 16) the posterior extremity of the
supraorbital ridge ends rather abruptly, as in Kumada and Hiyama’s figure of H. francisci
(my Text-figure 18, page 682). Some specimens of H. quoyi examined by me show vari-
ations in the form of the supraorbital ridge, as described later.
678 Bashford Dean Memorial Volume
Authors agree that in H. quoyi the origin of the first dorsal is well behind the root of
the pectoral. Garman states that the dorsal fins are of moderate size, with convex hind
margins; the base of the anal fin is two-thirds its length distant from the caudal; and the
anterior gill opening is more than twice as “wide” as the hindmost. Freminville states
‘that the skin is entirely shagreened, is colored a ruddy-brown and is everywhere strewn
with dark-brown spots, generally round. Concerning the coloration of H. quoyi Garman
(1913) writes:
Back rusty-brown, yellow below, with scattered spots of black, from mere specks to
spots as large as the orbit or larger, over the entire body and fins. Commonly the spots show
a tendency toward grouping in twos and fours; in [some] cases they are more confluent. On
some [specimens] there are five or six rather indefinite transverse bands of darker separated by
spaces of equal width; a band crosses the nape, another lies in front and a third behind the
first dorsal, one in front and one behind the second dorsal and one in front of the caudal.
A darker area extends from each orbit across the cheek.
It remains to record some observations on two specimens of H. quoyi, from the col-
lections of the American Museum of Natural History, which I have been permitted to
examine. The larger specimen is a female about 527 mm. (20.75 inches) long, measured
after 20 years’ immersion in alcohol. It is probably adult or nearly adult. This specimen
was collected on January 5, 1920, by Dr. R. C. Murphy, on the Lobos de Afuera Island
(off the coast of Peru) where it was washed ashore in a dying condition. The other
specimen is a male only 372 mm. (14.6 inches) long, and evidently very young. It was
taken on June 9, 1925, by Dr. R. C. Murphy at Albemarle Island of the Galapagos group,
from the stomach of a Tiger Shark (Galeocerdo). It seems in good condition after 15
years’ preservation in alcohol. Concerning these specimens it is necessary to consider
here only a few external characters, particularly those relating to the form of the body.
Certain details, including additional measurements, are left for a later section of the present
article entitled “Comparisons of H. quoyi and H. francisci”.
In the absence of published drawings of either dorsal or ventral views of H. quoyi
one is immediately impressed, upon examining these specimens, by the breadth of the
head and by the flatness of the ventral surfaces of both head and body. The outline of
the entire body, viewed from above, is quite tadpole-like. In the adult female the head
is much broader, proportionally, than in the young male. The head height of the young
male is greater, proportionally, than the head height of the adult female. In both speci-
mens the body height is greatest immediately in front of the first dorsal fin, where it
exceeds the height of the head sufficiently to give the fish a humpbacked appearance. In
its middle third, the supraorbital ridge is low and broad. In both specimens, this portion
is merely a fold of the skin not supported by the endoskeleton. In both specimens, the
external spiracular openings are small, measuring from 2 to 3 mm. in their larger diameters.
The first gill-slit is about twice the length of the fifth. The origin of the first dorsal is well
behind the posterior end of the pectoral base. The base of the anal fin is about three-fourths
its length from the caudal.
The Embryology of Heterodontus japonicus 679
In my 527-mm. female specimen of H. quoyi, the entire supraorbital ridge is low, but
it is lowest in its middle third where it is a mere fold of skin, not supported by the endo-
skeleton. This fold overlaps the eyeball like an upper eyelid. Its function is doubtless
protection of the eye while the fish is forcing its way under rocks or into crevices. When
pressed upon, this fold of the skin reduces the palpebral fissure to a narrow slit. Though
in all species of Heterodontus the supraorbital ridge leans outward, thereby overhanging
the eye, H. quoyi is probably the only species in which any part of it actually overlaps the
eyeball. In my adult female specimen of H. quoyi the supraorbital ridge does not end
abruptly, as it does in H. francisci.
In the same adult female specimen of H. quoyi, the “cheeks” appear swollen, and the
gill-covers, especially the first, bulge outward as if inflated by pressure from within. It
seems hardly likely that this condition could be produced by unequal shrinkage, since
it does not occur in other specimens preserved in the same way. As viewed from above,
the head is broad behind and somewhat pointed in front, like the head of a venomous
snake. The ventral surface of the head is decidedly flat, and lies in the same plane as the
ventral surface of the body. The nasal apertures open ventrad. As viewed from the side,
the dorsal surface of the head slopes forward toa fairly sharp rostrum directly in front
of the nostrils. The dorsal fins are small. The hind margin of the first dorsal is slightly
convex, that of the second dorsal is almost straight. The dorsal spines are decidedly small
but are much worn; they project less than a centimeter beyond the skin. The pectoral fins
are broad and when extended (as far as possible in their rigid condition) the distance from
tip to tip is about 250 mm., equal to nearly half the body length. The scales on the
ventral surface of the body are smooth; those on the dorsal surface are tuberculate and
are much larger than the scales on the ventral surface.
The form of my young specimen of H. quoyi (a male 372 mm. long) differs considerably
from that of the adult specimen (a female). Both head and body are more slender, especial-
ly in width. The ventral surface of the head is not so flat as in the adult. The supra-
orbital ridges are taller proportionally; they are especially well developed at their posterior
ends, where they terminate abruptly. Though the middle portion of each supraorbital
ridge is depressed, it overhangs the eye much less than in the adult. The dorsal fins are
proportionally larger, and the spines longer and sharper, than in the adult. The posterior
edges of both dorsals are so frayed that the original shapes of their margins cannot be
determined. It seems unlikely that any of the differences noted are due to sex. Some
characters, like the abrupt termination of the supraorbital ridges, may be individual vari-
ations, but most of the differences are probably correlated with differences in age.
In my two specimens of H. quoyi, the entire body, including the fins, is ornamented
with many dark-brown (nearly black) spots of various sizes. Of these, few are larger
than the orbit. These spots are occasionally grouped in twos, threes and fours. On the
dorsal surface there is a fairly regular bilateral arrangement of spots or groups of spots,
though in the large female the spots on that surface are more or less obscured by a dark-
brown ground color. On the ventral and ventrolateral surfaces the distribution is
680 Bashford Dean Memorial Volume
random, and the spots are distinct because the ground color is a light-brown. In the small
male specimen of H. quoyi the ground color is paler than in the adult female, so that the
spots are everywhere clearly visible. I do not find in either specimen the “‘fve or six
rather indefinite transverse bands” mentioned by Garman (1913). The spots on the
dorsal surface are distributed at fairly regular intervals in such fashion that when in-
distinct they might suggest broad transverse stripes; but such stripes would be more
numerous than those described by Garman.
Text-figure 17.
Jaws and teeth of Heterodontus quoyi, in lateral view. The original
is labelled Centracion quoyi.
After Garman, 1913, Atlas, Fig. 1, pl. 47.
JAws AnD TeeEtH.—In Garman’s figure (1913) showing the jaws of H. quoyi in
lateral view (my Text-figure 17) the upper jaw projects anteriorly beyond the lower jaw,
as in his figure of the jaws of H. phillipi drawn from the same aspect. Both jaws appear
very strong.
Some samples of both anterior and posterior teeth of H. quoyi are described and
sketched by Freminville; but Garman (1913, Atlas, Figs. 1 to 3, pl. 47) portrays the entire
dentition of both jaws. Authors agree that the anterior teeth are sharp and tricuspid,
with the middle cusp prominent. Garman records that the “molar” teeth are elongate,
narrow, each with a longitudinal ridge or keel. In Garman’s drawings the upper jaw has
11 transverse rows of anterior (cuspidate) teeth and 8 rows (4 on each side) of posterior
(grinding) teeth, making 19 rows in all. The lower jaw has 9 rows of anterior (cuspidate)
teeth and 6 rows (3 on each side) of posterior (grinding) teeth, making 15 rows in all. In
The Embryology of Heterodontus japonicus 681
general, the dentition resembles that of a half-grown specimen of H. phillipi. The anterior
teeth of my adult female H. quoyi are tricuspid with the middle cusp prominent; but the
anterior teeth of my young male specimen are quincuspid.
HETERODONTUS FRANCISCI GIRARD
This species has been taken off the coast of California and the western coast of
Mexico—especially in the Gulf of California. It was first described by Girard (1856).
The external form of the body has been figured by Maclay and Macleay (1879); Jordan
and Evermann (1900, Fig. 9, pl. III); Jordan (1905, vol. 1, Fig. 315); Daniel (1934, Fig. 17);
Kumada and Hiyama (1937, pls. 44 and 45). The best figures are probably those
of Kumada. His figures of a 540-mm. female are reproduced as Text-figures 18 and 19.
Girard’s description of Heterodontus francisci (which he calls Cestracion francisci) is
limited to a single paragraph, which I quote in full:
The largest of these specimens now before us, and measuring nearly two feet, bears a very
strong resemblance to C. phillipi, though of a somewhat more bulky appearance. The bony
ridge, above the eye, is much more developed, and the fins are larger also. The posterior
margin of the caudal is bilobed instead of being rounded: an emargination corresponding to the
top [sic] of the vertebral column. The anal is placed farther back; its tip projecting beyond
the anterior margin of the inferior lobe of the caudal. The posterior extremity of the ventrals ~
[pelvics] extends beyond the anterior margin of the second dorsal. Color, above yellowish-
gray, darker in the young; beneath light yellow. Small roundish-black spots are spread all
over the body and fins.
Girard’s comparison of the caudal fin of H. francisci with that of H. phillipi is based
on Lesson’s erroneous figure. The emargination corresponds to the tip, not the “top”, of
the vertebral column.
Some other points in which this species differs from H. phillipi are mentioned by
Maclay and Macleay (1879) whose account differs in some respects from Girard’s.
Their drawings were made from an adult male H. francisci, 708 mm. (27.9 inches)
long, from the Bay of Monterey, California. Dorsal and lateral views of the entire fish
are shown, but without spots—perhaps the specimen had been long in alcohol. In the
lateral view the pectoral and pelvic fins are not well displayed. As compared with H.
phillipi, the head is proportionally broader and less high; its profile is less steep and more
convex; the supraorbital ridges are less prominent, continuing almost to the snout and
terminating abruptly behind the eyes. The spiracle is larger and farther from the eye.
The first gill-opening is scarcely twice the length of the fifth. The dorsal spines are very
strong and are more than half the length of the dorsal fins. The dorsal fins themselves are
more broadly rounded at the apex and slightly emarginate behind.
Garman (1913) states that the color of H. francisci is grayish or olivaceous-brown
with small scattered spots of black over body and fins. On large specimens the spots are
sometimes absent or nearly so. The body is yellowish beneath. In the figures by Jordan
(1905) and by Daniel (1934) a few small roundish-black spots of fairly uniform size are
scattered over the entire body including the fins, and the supraorbital ridges differ from
682 Bashford Dean Memorial Volume
Textfigure 18.
Lateral view of a 540-mm. (21-inch) female specimen of Heterodontus francisci Girard.
After Kumada and Hyama, 1937, pl. 44.
those described by Maclay and Macleay (1879) and by Garman (1913) in not ending so
abruptly behind the eyes.
The principal external characters of an adult or nearly adult female H. francisci are
well illustrated in my Text-figures 18 and 19, after Kumada and Hiyama (1937). These
authors state that this shark, which is abundant in their collection, scarcely exceeds two
feet in length. The body is brown, the belly much fainter. Small round black spots are
Text-figure 19.
Dorsal view of the 540-mm. (21-inch) female specimen of Heterodontus francisci Girard, shown in
lateral view in Text-figure 18.
After Kumada and Hyama, 1937, pl. 44.
The Embryology of Heterodontus japonicus 683
scattered all over the body and fins. The authors list this species under the generic name
Gyropleurodus.
To Kumada and Hiyama (1937) we are also indebted for figures representing dorsal
and lateral views of a young female H. francisci about 240 mm. (9.84 inches) long. In this
specimen, the supraorbital ridges are low in the middle third, as in the two specimens,
respectively young and adult, of H. quoyi examined by me. The color pattern of the
young specimen of H. francisci figured by Kumada differs from that of adults of this
species. The spots are larger and more complex; on the dorsal surface they are arranged
according to a definite pattern. The spots are more numerous on the dorsal surface than
on the lateral and ventral surfaces; on the fins, excepting the caudal, they are either in-
distinct or absent. Each spot consists of a very dark central portion surrounded by
a moderately dark zone. On the dorsal surface of head and body, the very dark spots
are grouped in about ten transverse rows, each imbedded in a moderately dark
stripe. On the body these stripes, each with its enclosed darker spots, are crescentic in
outline, the concave margin facing forward; but on the head there are, anteriorly, two
straight transverse stripes and, posteriorly, one crescentic stripe with its concave margin
facing caudad. Collectively, these transverse stripes form a pattern which is bilaterally
symmetrical with respect to the dorsal mid-line of the body.
The skeleton of H. francisci has been described by Daniel (1914 and 1915). From
his figures it appears that the vertebral column is better developed and the notochord is
more constricted in Heterodontus than in Heptanchus (Daniel, 1934) and Chlamydoselachus
(Goodey, 1910, reviewed by Smith, 1937).
My material for the study of H. francisci consists of two female specimens (one is
an adult) collected by Dr. C. H. Townsend of the Albatross Expedition of the American
Museum of Natural History on April 10, 1911, at Angel de la Guardia Island, Gulf of
California. The larger specimen is about 705 mm. (27.75 inches) long, and the smaller
one 565 mm. (22.25 inches). Some additional measurements, for comparison with H.
quoyi, are given on page 684.
The two specimens of H. francisci are much alike. In both, the head including the
gillregion is broad, but in the larger fish it is broader in proportion to the total length.
In the smaller and presumably younger specimen, the height of the head, in proportion to
its width, is greater. The larger shark has a decided hump between the head and the
first dorsal fin, but a similar hump on the smaller fish is less conspicuous. In both speci-
mens, the supraorbital ridges are rather tall. They are supported throughout their
length by the endoskeleton, and they terminate rather abruptly at their posterior ends.
The length of the first gill-slit is about double that of the fifth, as in H. quoyi. The
spiracular openings are comparatively large: in the larger specimen their longer diameter
is from 4 mm. to 5 mm., in the smaller fish 3 mm. to 4mm. Dorsal fins and dorsal spines
are larger than in H. quoyi. In both specimens, the origin of the first dorsal is directly
above the posterior margin of the pectoral base (as in Garman’s H. japonicus). The hind
margins of both dorsals are concave. The base of the anal fin is slightly more than its
68+ Bashjord Dean Memorial Volume
length distant from the caudal. The scales on the dorsal surface of the body are not
particularly large. A few dark spots are visible; these are small, widely scattered, and
most of them were found only after a careful scrutiny.
Jaws anp TreTH—In his “Atlas” (1913) Garman figures teeth and jaws of very
young, medium-sized and adult specimens of H. francisci. In his figure showing the
jaws in lateral view, they bear a close resemblance to those of H. quoyi (my Text-figure 17).
In Daniel’s figure of the skull of H. francisci (1915, Fig. 6, pl. III) the form of the jaws as
seen in lateral view is somewhat intermediate between the two quite different forms
portrayed by Goodrich (my Text-figure 33) and Garman (1913; Fig. 4, pl. 47) for H.
phillipi. One infers that these differences are individual and not specific.
Maclay and Macleay (1879) state that the front teeth of H. francisci are strongly
tricuspid, those at the sides are longitudinally ridged. Garman (1913) wnites that the
anterior teeth have five cusps, the middle one the longest; with age the outer cusps
become less apparent and the middle cusps much stronger. His drawings show the
posterior teeth longitudinally ridged in all stages. In my two large female specimens
the anterior teeth are tricuspid.
COMPARISON OF HETERODONTUS QUOYI AND FRANCISCI
In my descriptions of the specimens of H. quoyi and H. francisci belonging to the
American Museum of Natural History, some statements were made concerning the form
oi the body. It seems desirable to bring together the data upon which these statements
were based, in order that certain features in the two species may be accurately compared.
Incidentally, a few comparisons will be made with other species.
The measurements upon which the present discussion is based are given in Table
In this connection one should bear in mind that the female specimen of H. quoyi is presum-
TABLE I
SOME MEASUREMENTS IN MILLIMETERS OF FOUR SPECIMENS OF HETERODONIUS
| Species H. quoyi H. jrancsa
Female | Male Female | Female
527 372 705 365
118 6 | 138 S7
& 41 86 67
80 48 110 75a
30 is 34 |
4 S 17 14 eal
| 25 12 ) o. |
28 is 42 32
of anal $n and veniral Jobe of caudal... ...-....-...---.-- 34 23 43 33
| j
ably adult or nearly adult, while the male of the same species is decidedly young. The
larger specimen of H. francisci is known to be adult.
I may say at once that the two species are readily separable. In certain features of
The Embryology of Heterodontus japonicus 685
their external anatomy they differ so much that they are distinguishable at a glance; but
I suspect that even a gifted artist could not portray all their subtle and almost intangible
differences of contour.
In both species the head is broader than the body (excluding the paired fins). The
region of greatest breadth lies between the first gill-covers. In the large female specimen
of H. quoyi, the greatest breadth equals 22.3 per cent of the total length; in the decidedly
small and immature male specimen of the same species, only 16.1 per cent. In the larger
female specimen of H. francisci, the greatest breadth equals 19.5 per cent of the total
length; in the smaller female of the same species, only 17.1 per cent. It is apparent that in
both species the breadth of the head, in proportion to total length, is greater in the older
specimen; but when allowance is made for age (ignoring sex as a possible factor) H. quoyi
is definitely broader than H. francisci. For further information we must have recourse to
published drawings, which are not so satisfactory as specimens since we have no assurance
that they were made from accurate measurements. There are no drawings of either
dorsal or ventral views of H. quoyi. In Maclay and Macleay’s dorsal view (1879) of
their 708-mm. specimen of H. francisci, the greatest breadth (which is in the region of the
first gill-covers) equals 17.5 per cent of the total length—a proportion somewhat smaller
than that obtained for my larger specimen of H. francisci, which has almost exactly
the same length.
It may be of interest to extend this comparison to other species, but there we must
depend entirely on drawings which may not be made to scale. Maclay and Macleay’s
dorsal view of a full-grown specimen of H. phillipi (my Text-figure 7, page 667) has
a head that appears broad as compared with most sharks, but is decidedly narrower than
the heads of my adult specimens of H. quoyi and H. francisci. Maclay and Macleay’s very
young specimen of H. phillipi (my Text-figure 9, page 669) has a head that is much
narrower than that of their adult of the same species. In a young female specimen of H.
zebra described and figured by Maclay and Macleay (1886) the width of the head cannot
be measured because in the dorsal view the head is turned slightly to one side; but it
appears very narrow, and the entire body is narrow as compared with other species of
Heterodontus. Ina drawing by Maclay and Macleay representing a dorsal view of a young
female specimen of H. japonicus about 406 mm. long (my Text-figure 24, page 691), the
width of the head equals 15.7 per cent of the total length. This is slightly narrower
than the head of my young male specimen of H. quoyi, and of course much narrower than
the heads of adult specimens of H. quoyi and H. francisci.
In my adult female specimen of H. quoyi, the height of the head (including the
supraorbital ridge) equals 54.2 per cent of its breadth, while in my young male of the same
species the proportion is 68.3 per cent. In my larger female specimen of H. francisci
the height of the head equals 62.3 per cent of its breadth; in the slightly smaller female
of the same species the corresponding percentage is 69.0. We do not know if sex is
a factor in determining the size or bodily proportions in these species, so this possibility
must be ignored. With this reservation, the data indicate that in the adults of both
686 Bashford Dean Memorial Volume
species the head is dorsoventrally depressed, but more so in H. quoyi than in H. francisci.
In both species, during growth the head becomes broader and less tall proportionally, but
only the ventral surface becomes actually flat. Because of differences in the shape of the
head, its bulk in the two species cannot be compared by ordinary measurements.
From the total evidence it appears that most species of Heterodontus, in adaptation to
a bottom-dwelling mode of life, have differentiated moderately in the direction of a broad-
ening of the head and anterior part of the body, accompanied by a lessening of the head
height and a flattening of the ventral surface of both head and body. These features
emerge in the course of development after hatching, and are not found in the very young—
a circumstance which leads us to infer that the more or less remote ancestors of this group
were not bottom-dwelling forms. From the meager information available, it is possible
that H. zebra has evolved in a different direction, tending to become eel-like in form.
This, also, is an adaptation to life on the ocean bottom.
Another feature common to my specimens of both H. quoyi and H. francisci is the
slightly humpbacked appearance. This has already been mentioned as a possible generic
or family character. The hump is not due to an arched condition of the body. In each of
my specimens the greatest height of the dorsal surface, excluding the dorsal fins, occurs in
the region above the fifth gill-slit, which is also above the base of the pectoral fin. In the
pectoral region the ventral body wall is frm and the height of the body may be measured
accurately. The height of the hump may be computed by subtracting the head height
from the body height. Comparison of the height of the hump, in proportion to body
height in different specimens, may be made on a percentage basis. In my large female
specimen of H. quoyi the height of the hump equals 20 per cent of the body height; in the
small male specimen of the same species, 14.5 per cent. In the larger female specimen of
H. francisci the excess of body height over head height equals 21.8 per cent of the body
height; in the slightly smaller female, 10.6 per cent. It is noteworthy that in H. francisci
the smaller of two large female specimens has a hump only half the height of the other.
Judging from the drawings that have been published, this variability occurs also in H.
phillipi and H. japonicus.
HETERODONTUS GALEATUS GUNTHER
The range of H. galeatus, so far as known, is limited to the waters of Queensland
and New South Wales. Whitley (1940) writes that in the northern part of New South
Wales this species (which he calls Molochophrys galeatus) tends to replace H. phillipi.
H. galeatus was first described, from a single specimen, by Giinther (1870). The
first drawings of the entire fish are those of Maclay and Macleay (1879); they comprise
lateral, dorsal and frontal views. These drawings were made from a stuffed female
specimen (length not given) in the Australian Museum. A much better portrayal of
a lateral view, published by Whitley (1940), is here reproduced as Text-figure 20. Whitley
records that the length of sharks of this species is about five feet. Presumably this refers
to adult specimens.
The Embryology of Heterodontus japonicus 687
Text-figure 20.
A female specimen of Heterodontus galeatus Gunther captured off Sandon Bluff, New South Wales, Australia.
The inset figure shows the mouth opening, the nares, oro-nasal grooves, labial folds and some of the front teeth.
After Whitley, 1940, Fig. 56, p. 73. i
The most outstanding peculiarity of this species is the unusual height of the supra-
orbital ridges. These ridges approach each other anteriorly, and diverge posteriorly;
they end abruptly a short distance behind the eye. Garman (1913) says that they end ab-
ruptly in young specimens, less so in old. As shown ina frontal view by Maclay and
Macleay (1879) the ridges lean outward (laterad) at an angle of about 45 degrees from the
median plane. Waite (1898 and 1899) and Whitley (1940) refer to this shark as
the “crested species”. The name Crested Shark seems appropriate, though it might with
some justice be applied to any species of Heterodontus. The name “Crested Port Jackson
Shark”’’, used by Whitley, seems inadmissable.
Garman (1913) states that the form of H. galeatus is similar to that of H. francisci, but
the head is short and angular. The anterior gillopening is more than twice as “wide”
(presumably meaning high or long) as the hindmost. The origin of the first dorsal fin is
above the hinder part of the pectoral base; the hind margin of the first dorsal is concave.
The base of the anal finis about two-thirds of its length distant from the lower lobe
of the caudal.
The color pattern is not well shown in Maclay and Macleay’s lateral view (1879),
but is quite distinct in their dorsal view of the same specimen. Six broad transverse dark
stripes are said to be visible, but in the drawing the most posterior stripe is very faint.
Garman (1913) states that the general color is brown, with a transverse stripe of darker
across the orbits, widening upon the cheek; another band in front and one behind the
ventrals (pelvics); one through the second dorsal and one in front of the anal, less definite
than the anterior—making five instead of six as enumerated by Maclay and Macleay. The
688 Bashford Dean Memorial Volume
color pattern is not very distinct in Whitley’s figure (1940) reproduced as my Text-figure
20. Whitley states that the color is light-brownish, with the interorbital region and the
back in front of (the first?) dorsal fin blackish; a broad blackish bar below the eye; back
with some dark transverse bars, one at base of each dorsal fin most prominent, but not
joining to depict a “harness”. This shark sometimes becomes stained a reddish color on
teeth or skin apparently through eating the purple sea urchins of Australian harbors.
At the time when Maclay and Macleay’s description was written (1879), only two
specimens of H. galeatus were known: the stuffed specimen in the Australian Museum,
and Dr. Giinther’s specimen in the British Museum. Maclay and Macleay wrote that it
was not at all improbable that the fish might not, after all, be of such very rare occurrence.
“The general resemblance to H. phillipi is considerable, and fishermen are generally far
from being acute observers of fish which are not of a marketable character.” Ogilby
(1890) wrote that, at Port Jackson, the species was almost as common as H. phillipi. He
stated that he had also received specimens from Port Stephens, New South Wales.
Waite (1898) made extensive collections of marine fishes in the waters adjoining New
South Wales, including specimens of H. phillipi from 14 different stations. Concerning H.
galeatus he wrote: “Although a careful lookout was kept for the crested species,
Heterodontus galeatus, it was never taken and notwithstanding this fact, all the egg cases
I saw southward in the shop windows of Wollongong and Kiama were of the latter species
[galeatus|, those of our commoner form (phillipi) being either rare or quite unknown”.
TrEeTH.— Waite (1899) published a photograph of the teeth of both upper and lower
jaws of H. galeatus (which he called Gyropleurodus galeatus) and stated that the teeth
portrayed by Maclay and Macleay (1879, Figs. 30 and 31, pl. 25) and attributed to H.
galeatus, were not of that species. The differences in the figures of the posterior teeth
are very marked. In Waite’s figure the posterior or grinding teeth are much smaller,
more nearly uniform in size and more numerous. In Maclay and Macleay’s figure they do
not differ materially from those portrayed, by various authors, for other species, except
that they are more elongate. In one respect the figures of the posterior teeth by Waite
and by Maclay agree: the longitudinal ridge is distinct, perhaps stronger than in any
other species. My general impression is that the teeth of H. galeatus figured by Waite
are more primitive (in that the posterior or grinding teeth do not differ so much from the
anterior or cuspidate teeth) than the teeth of any other species of Heterodontus.
HETERODONTUS JAPONICUS MACLEAY
For many years, specimens of Heterodontus collected in Japanese waters were classi-
fied as Cestracion (Heterodontus) phillipi, the Port Jackson Shark. Thus the specimens
figured and described under this name by Muller and Henle (1841) and by Brevoort (1856)
were collected in Japan. Also Siebold (1850, in his “Fauna Japonica”’) stated that a shark,
which he called Cestracion phillipi, was very common during spring and summer along the
southwestern coast of Japan, especially in the Bay of Nagasaki. He wrote that it attains
a length of three feet and that it was much sought after for food by the Japanese. There
The Embryology of Heterodontus japonicus 689
is now no doubt that the species of Heterodontus ordinarily taken in Japanese waters is
not H. phillipi but a different species, named by Macleay (in Maclay and Macleay, 1879)
Heterodontus japonicus. A related species, H. zebra, has been taken but rarely in Japanese
waters, and there is no authentic record of H. phillipi ever having been taken off Japan.
Thus the English common name, Japanese Bullhead Shark, seems appropriate for Hetero-
dontus japonicus.
As stated early in this article, Dean collected eggs and embryos of H. japonicus in
the Sagami Sea, at the entrance to the Gulf of Tokyo. In his notes Dean states that this
shark is not uncommon along the coasts of the Japanese islands south of Hokkaido. In
certain regions it is known to be abundant, as along the shores of the Inland Sea and in the
Sagami Sea.
The Japanese Bullhead Shark has received several local names. Siebold (1850)
stated that the local name was Sasiwari. Brevoort (1856) explains that this name is
doubtless derived from Sas-ir, to stick in, and war, to cleave—in allusion to the spines in
front of the dorsal fins. Jordan, Tanaka and Snyder (1913, p. 8) record the following
colloquial names: Nekozame (Tokyo market; Misaki; Sagami); Sazaewari (Prov. Shima;
Osaka; Prov. Tosa); Sazaiwari (Nagasaki). It is called ““Nekozame” in the volume entitled
““TIlustrations of Japanese Aquatic. .. Animals” (1913) elsewhere referred to. Dr. Dean
calls it Nekozamé. A synonymy of scientific names follows:
HETERODONTUS JAPONICUS Macleay
Cestracion phillipi. Miller and Henle, 1841, Plagiostomen, p. 76, pl. 31.
Cestracion phillipi. Siebold, 1850, Fauna Japonica: Pisces, p. 304.
Heterodontus zebra (not Gray). Bleeker, 1854, Verh. Bat. Gen., 26, 127.
Cestracion phillipi. Brevoort, 1856, Perry Expedition, vol. II, Fig. 2, pl. 12.
Cestracion phillipi var. japonicus. Duméril, 1865, Elasm., p. 426.
Cestracion phillipi. Ginther, 1870, Cat. Fishes Brit. Mus., vol. VIII, p. 415.
Heterodontus japonicus Mcl. Maclay and Macleay, 1884, Proc. Linn. Soc. New South Wales,
8, p. 428, pl. XX.
Heterodontus japonicus Mcl. Steindachner, 1896, Ann. K.K. Naturhist. Hofmus., Wien, 11,
p. 224.
Heterodontus japonicus. Jordan and Fowler, 1903, Proc. U.S. Nat. Mus., 26, p. 599.
Cestracion japonicus (Duméril). Regan, 1908, Ann. Mag. Nat. Hist., 8. ser. 1, p. 496.
Centracion japonicus. Garman, 1913, Plagiostomia. Mem. Mus. Comp. Zool., 36, p. 184.
Heterodontus japonicus Duméril. Jordan, Tanaka and Snyder, 1913, Journ. Coll. Sci., Imp.
Univ. Tokyo, 38, Art. 1, p. 8.
The Japanese Bullhead Shark, Heterodontus japonicus, was first figured and described
by Miller and Henle (1841). Their specimen and figure were labelled ““Cestracion
phillip’. At the time when their monograph was published, only three species of
Heterodontus (Cestracion) were known: H. phillipi, H. zebra and H. quoyi. No evidence
other than the figure itself (my Text-figure 21) is necessary to prove that the specimen
drawn was not one of these. Miller and Henle listed nine specimens of H. phillipi
stored in various museums, and stated that they were collected in ““Neuholland” (now
690 Bashford Dean Memorial Volume
Text-figure 21.
A male Japanese Bullhead Shark, Heterodontus japonicus Macleay, length not recorded. The original figure
is in color and is labelled Cestracion phillipi.
After Miller and Henle, 1841, pl. 31. Right and left are here reversed.
Australia) and in Japan. But Heterodontus phillipi does not occur in Japanese waters.
Moreover, Siebold (1850, p. 304) noted that the Muller and Henle figure was drawn by
Burger from a fresh specimen collected in Japan.
A specimen of H. japonicus described and figured by Brevoort (1856) was labelled
“Cestracion phillipi’. This specimen (my Text-figure 22) was collected at Simoda
Textfigure 22.
A very young (recently hatched) male Japanese Bullhead Shark, Heterodontus japonicus, collected by the
Perry Expedition to Japan. The original figure, from a recently procured specimen only 216 mm. (8.5 inches)
long, is in color and is labelled Cestracion phillipi.
After Brevoort, 1856, pl. XII.
The Embryology of Heterodontus japonicus 691
Text-figure 23.
A young female Japanese Bullhead Shark, Heterodontus japonicus. This specimen, collected in Japanese
waters, was about 406 mm. (16 inches) long, and was drawn after preservation in alcohol.
After Maclay and Macleay, 1884, Fig. 1, pl. 20. Right and left are here reversed.
(Shimoda, at the entrance to the Sagami Sea?) by the Perry Expedition to Japan. Brevoort
states that all the drawings of fishes were made from recently procured specimens; but
that no professional zoologists accompanied the expedition, hence in making the drawings
no close attention was paid to specific characters. From the small size of Brevoort’s
Text-figure 24.
Dorsal view of the 406-mm. (16-inch) preserved female specimen of Heterodontus japonicus shown in lateral
view in Text-figure 23. The inset figure is an outline of a front tooth.
After Maclay and Macleay, 1884, Figs. 2 and 5, pl. 20.
692 Bashford Dean Memorial Volume
specimen (only 216 mm. or 8.5 inches long) one infers that it must have been recently
hatched. Brevoort’s description of the color and color pattern follows:
Its general color is of a pale sepia-like brown, darker on back and fins, with a pinkish
tinge on lower parts of the body. Irregular bands and large blotches of several shades of the
same brown are distributed from the pectorals to the caudal, grouped in five principal bands,
with smaller ones near the back between the first three large ones. The first of these last is
just back of the pectorals, the second back of the first dorsal and in front of the ventrals,
spreading laterally near the abdomen. The snout and cheeks are shaded also with darker-brown
cloudings. Small pale-brown dots, besides the above, cover the back of the head and body
and about one-half of the pectorals, dorsals and caudal. Ventrals, anal, and lower lobe of
dorsal of a more uniform brown.
The first specimen to be described, figured and labelled Heterodontus japonicus is
that of Maclay and Macleay (1884). This specimen is a 406-mm. (16-inch) female obtained
from Japan; it is evidently not fullgrown. The authors state that the “coloration and
markings” of their specimen are not by any means distinct, the fish having been long in
spirits; but the remains of numerous dark-brown bands across the back present a very
different style of marking from those of the other known species of the genus. Maclay
and Macleay’s drawing of the entire fish in lateral view (my Text-figure 23) shows the
transverse dark bands with eSsentially the same distribution as in Muller and Henle’s
figure, save that the band immediately in front of the first gill-slit is lacking. In their
drawing of the same specimen in dorsal view (my Text-figure 24) the transverse bands
are more prominent.
Maclay and Macleay’s further description of their 406-mm. (16-inch) female specimen
of Heterodontus japonicus is here given very nearly in the words of the authors, but with
some rearrangement and clarification. They state that the snout is very bluntly rounded
(my Text-figures 23 and 24). The mouth (Text-figure 25) differs from that of H. phillipi
in having the inner nasal fold less long, the fold of the upper lip rounder and shorter, and
the inferior margin of the fold of the lower lip covered with soft skin having only a very
few scutellae (placoid scales). The spiracle (Text-figures 23 and 24) is distinct, and larger
than in H. phillipi. It is placed a little below and behind the eye. The lateral line is
straight and continuous from the supraorbital ridges. The first dorsal fin is high and
Text-fhigure 25.
Anterior part of the head of Heterodontus japonicus
seen from the ventral side, showing the mouth open-
ing, nares and oro-nasal grooves, the labial folds and
some exposed anterior teeth. From the young female
specimen about 406 mm. (16 inches) long, shown in
Text-figure 23 and 24.
After Maclay and Macleay, 1884, Fig. 3, pl. 20.
The Embryology of Heterodontus japonicus 693
falciform; the height is exactly twice the length of the portion of the base attached to the
back. The spine is small and acute (as compared with that of H. phillipi), being only half
the length of the fin. The second dorsal is shaped like the first, but is less in height, and
its base of attachment to the back is about the same. The distance between the two
dorsals is equal to that between the second dorsal and the commencement of the caudal
fin, and to that between the first dorsal and the eye. The pectorals are large and tri-
angular, and about equal in length to the caudal. The ventrals (pelvics) are situated in
a line intermediate between the two dorsals. The anal commences distinctly behind the
second dorsal, and does not nearly reach the caudal. The lower lobe of the caudal is very
deeply and less than rectangularly notched. The authors do not mention the hump on the
anterior part of the body, which is quite prominent in their figure representing a lateral
view (my Text-figure 23).
To Bashford Dean we are indebted for the only photograph of a fresh-caught adult
Japanese Bullhead Shark on record. This was published (Dean, 1904) in the Popular
Science Monthly in an article entitled ““A Visit to the Japanese Zoological Station at
Misaki” and is reproduced herein as Text-figure 3. page 655. The original legend reads
‘A Freshly Caught Port Jackson Shark”’, but since Dean states in the accompanying text
that a Port Jackson Shark is abundant at Misaki, it is evident that he was using the name
in a generic, not a specific sense—for Heterodontus phillipi does not occur at Misaki.
Thus the species is almost certainly H. japonicus, though H. zebra, a more slender form,
does occur somewhat rarely in the vicinity of Misaki. The photograph does not show the
color pattern, which would make identification easy. In Dean’s photograph, one must
make some allowance for the trick of the camera in enlarging objects in the foreground:
the pectoral fin is probably a little too large. Since the mouth is partly open, the lower
jaw has sagged and the cranium is slightly upraised.
Ameng Dean’s records there is a faded photograph showing a dorsal view of an
adult or nearly adult Heterodontus, presumably japonicus. The supraorbital ridges are
well shown. They are strongly upraised, though narrow, and approach each other at
their anterior ends, diverging posteriorly. At their posterior ends they terminate
rather abruptly, though not so abruptly as in H. galeatus (Text-figure 20 and in Maclay
and Macleay’s lateral view). The breadth of the head, measured between the first pair of
gill-covers, equals 19 per cent of the total length. The pectoral fins are extended, and the
distance from tip to tip equals 56 per cent of the total length.
A young female specimen of Heterodontus japonicus in the collections of the American
Museum of Natural History measures about 280 mm. (eleven inches) in length “‘over all”.
It is described on page 757 and portrayed in Text-figure 65, of the present article.
There remains to be considered a figure of the Japanese Bullhead Shark contained in
a folio volume entitled “Illustrations of Japanese Aquatic Plants and Animals”, published
by the Japanese Fisheries Society in 1931. An adult specimen of Heterodontus japonicus
is there portrayed in color. Upon comparing this figure with those of other authors
(including the photograph by Bashford Dean reproduced in my Text-figure 3) one gets
694 Bashford Dean Memorial Volume
Text-figure 26.
Dentition of Heterodontus japonicus: A, upper
jaw; B, lower jaw. Drawn from the young female
specimen, 406 mm. (16 inches) long, shown in
Text-figures 23 to 25.
After Maclay and Macleay, 1884,
Figs. 4a and 43, pl. 20.
an impression that it is inaccurate in several
respects. The eye is too large and too near
the top of the head; the supraorbital ridge is
omitted or represented as part of a circular
ridge extending entirely around the eye. The
notch in the ventral lobe of the caudal fin is
curved instead of angular. The dark brown
transverse stripes are more regular and less
numerous than in any other drawing of this
species. For these reasons this figure is not
reproduced here. The legend states that the
species is not good for food—contrary to the
statement in Siebold’s “Fauna Japonica”. “De
gustibus non est disputandum’.
TeetH.—In Maclay and Macleay’s young
(16-inch) female specimen of the Japanese Bull
head Shark, there are 23 transverse rows of
teeth in both upper and lower jaws (my Text-
figure 26). The anterior (cuspidate) teeth are
K typically fve-cusped. In the upper jaw, the
number of teeth in the central row is eight (one
is not visible in Text-fgure 26). In the lower
jaw, the transition between anterior (cuspidate)
and posterior (grinding) teeth is very abrupt;
in the upper jaw it is more gradual. In making
comparisons with the teeth of other Hetero-
dontid sharks, it should be borne in mind that
Maclay and Macleay’s description is based on
a single specimen, and that this specimen was a
decidedly young one.
The development of the teeth of Hetero-
dontus japonicus is further described in the final
section of this article, which contains also a
concise summary of the main course of develop-
ment of the teeth of the entire genus.
AFFINITIES TO FOSSIL FORMS
In the introduction to this article I have
pointed out that the genus Heterodontus in-
cludes some fossil forms, so that the paradoxi-
cal term “living fossils” might pardonably be
The Embryology of Heterodontus japonicus 695
Text-figure 27.
Hybodus hauffianus E. Fraas: skeleton, with skin (shagreen) outlining the entire body which is about
2240 mm. (88 inches) long. Upper Lias; Holzmaden, Wurttemberg.
After Koken, 1907, Taf. I.
applied to present-day representatives of the group. Of greater importance is the close
relationship between the Heterodontidae and the Hybodontidae, which will now be
discussed. Since paleontologists almost uniformly use the term Cestracion instead of
Heterodontus, and Cestraciontidae in place of Heterodontidae, it is advisable, in review-
ing their work, to adopt their language without a tiresome repetition of synonyms.
In his “‘Catalogue of the Fossil Fishes in the British Museum”, Woodward (1889)
defined the Cestraciontidae very broadly as follows: ‘Dorsal fins each armed with a spine,
the first opposite to the space between the pectoral and pelvic fins. Teeth mostly obtuse,
never fused into continuous plates; several series simultaneously in function”. He
further states that ‘No distinctive characteristics of value having yet been discovered,
the so-called Orodontidae and Hybodontidae are included in this family”.
This classification, or something like it, seems to have been adopted by Goodrich
(1909) since he includes Orodus and Hybodus (the latter portrayed in my Text-figures 27
and 28) in the family Cestraciontidae. Regan (1906) had already separated the Ces-
traciontidae from the Hybodontidae. Most of the characters that Regan lists for the
two families are identical, but he states that in the Cestraciontidae the pterygoquadrate
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Reconstruction of the skeleton and outline of the body of Hybodus hauffianus E. Fraas, based on a
specimen about 1220 mm. (48 inches) long. Upper Lias of Holzmaden, Wurttemberg.
After Jaekel, 1906, Fig. 2.
696 Bashford Dean Memorial Volume
(palatoquadrate) has a preorbital articulation with the cranium, while in the Hybodontidae
the attachment is postorbital. Nine genera, including Paleospinax and Synechodus, were
assigned to the Hybodontidae, leaving one genus, Cestracion, for the Cestraciontidae.
In the second German edition of his ““Grundztige der Palaeontologie”’, Zittel (1911)
listed in his family Cestraciontidae seven genera including Cestracion. Eight other genera,
including Hybodus and Orodus, made up his family Hybodontidae. The most recent
(fourth) German edition of Zittel (1923) departs only slightly from this classification. In
the separation of the two families, Woodward appears to have taken part. In the second
English edition of Zittel, revised by Woodward in 1932, the family Cestraciontidae
includes only three genera (Cestracion, Paleospinax, and Synechodus) while the family
Hybodontidae comprises thirteen genera including Hybodus and Orodus. Woodward’s
definitions of the two families deserve careful attention:
DISTINCTIVE CHARACTERS OF THE HYBODONTIDAE AND THE CESTRACIONTIDAE
According to Woodward in Zittel (1932).
HYBODONTIDAE
Teeth numerous, mostly obtuse, never
fused into continuous plates; several series
simultaneously in function. Notochord
persistent. Some ribs long and slender;
neural arches also long and slender. Each
of the two dorsal fins armed with a spine,
which is as deep as the fin; the spine orna-
mented on the sides and bearing one or two
CESTRACIONTIDAE
Teeth as in Hybodontidae. Vertebral
centra cyclospondylic or asterospondylic.
Ribs and neural arches very short and broad.
Each of the two dorsal fins armed with
a spine which is less deep than the fin; the
spine is almost or completely unornamented,
and without posterior denticles. Anal fin
without spine. Tail heterocercal. No head
rows of posterior denticles. Anal fin with-
out spine. Tail heterocercal. Paired
hooked head spines often present. Devonian
or Lower Carboniferous to Cretaceous.
spines. Lower Jurassic to Recent.
Several of the characters listed above are much alike in the two families. The degree
of this likeness, and its significance, need some evaluation; but first let us note some pos-
sible additions to the list of resemblances. Certain peculiarities in the form of the head
and anterior part of the body of some Cestracionts, leading to the common name “Bull
head Sharks”, find a counterpart in fossil forms like Hybodus (Text-figures 27 and 28).
This matter has been discussed on pages 660 and 686. A considerable degree of flatness of
the ventral surfaces of both head and body may also be common to the two families.
Woodward (1921) states that in their general appearance the Hybodonts resemble the
Cestracionts. The pectoral girdles of both Heterodontus (Daniel, 1915, Fig. 8, pl. IV)
and Hybodus (my Text-figures 27 and 28) are very strong.
Some of the characters common to the two families are included in the definitions
presumably for comparison with other families in the same suborder, or to show inclusion
The Embryology of Heterodontus japonicus 697
Text-figure 29.
Teeth of Hybodus, outer aspect, natu-
ral size: A, three associated teeth of
Hybodus delabechei Charlesworth; B,
three associated anterior teeth of
Hybodus reticulatus Agassiz.
After Woodward, 1889, Part 1, pl. X.
in some larger group; but we are here concerned mainly with the interrelations of the
two families. From this point of view, the descriptions of the teeth by Woodward are
inadequate when isolated from the special accounts of the teeth of the various genera.
There is considerable variation in the teeth of different genera in both families, and the
differences are of the same kind.
In Hybodus the teeth (Text-figures 29 and 30) are all cuspidate. In the anterior teeth
the cusps are more or less acute, with the central cusp predominant and the other cusps
somewhat irregular in size and number. In the posterior teeth there is a tendency toward
differentiation into grinders; for these teeth are larger than the anterior teeth and their
cusps are almost or quite obtuse. But in some other genera of the family Hybodontidae,
low rounded crushing teeth, slightly ridged and with only a few vestigial cusps, occur
(e.g., as in Orodus, figured by Eastman, 1903; and Acrodus, beautifully illustrated by
Woodward, 1889).
Similar differences occur in the three genera of the Cestraciontidae. The teeth of
Synechodus (Text-figure 31) are much like those of Hybodus (Text-figures 29 and 30)
Text-figure 30.
Posterior teeth of Hybodus, in natural sizes. A, Hybodus delabechei Charlesworth: four
posterior series of teeth, coronal aspect; one tooth of each of three series is shown also
in side view. B, Hybodus raricostatus Agassiz: two posterior series of teeth and portions
of a third, coronal aspect; two teeth are shown also in side view.
After Woodward, 1889, part 1, pl. X.
698 Bashford Dean Memorial Volume
Text-figure 31.
Dentition of Synechodus dubrisiensis Mackie, a member of the family Heterodontidae (Cestraciontidae)
represented only by fossils. These teeth are twice natural size, with six separate teeth enlarged four times.
Upper Cretaceous, Sussex.
After Woodward, 1889, Part 1, Text-fig. 12, p. 326.
except that the anterior teeth of Synechodus are larger than the posterior ones. The teeth
of Paleospinax show progress in the direction taken by Heterodontus: the few anterior
teeth are high-crowned and prehensile with only a single pair of lateral denticles, while
the posterior teeth are low-crowned with two or three pairs of lateral denticles reduced to
minute beads (Zittel, 1932). Finally in Heterodontus, the only genus represented by
living specimens, the anterior teeth of the adult are typically tricuspid, the central cusp
predominating; while the posterior teeth are large, and set in oblique rows, without
cusps but with the grinding surface of each tooth traversed by a slender longitudinal
ridge—unless this is worn away by use. Nearly complete skeletons of Heterodontus
(Cestracion) have been found in the Lithographic Limestone (Upper Jurassic) of Bavaria
and the Chalk of England. The teeth of these fossils, which include several extinct
species, are said to differ little from those of recent examples of the genus save that the
crowns of the grinding teeth are rugose in addition to having a longitudinal keel.
The spines of the dorsal fins are not limited to sharks of the families under consider-
ation, but one of the most obvious differences between the two families is the ornamenta-
tion of the dorsal spines in the Hybodontidae and the almost entire lack of it in the
Heterodontidae. The “‘ornamentation” consists of longitudinal ridges along the sides and
sometimes the front of the spine, and the presence of tubercles on its rear surface. In two
genera of fossil Heterodontidae, Paleosbinax and Synechodus, the dorsal fin spines are
almost uniformly smooth, and in Heterodontus they are entirely smooth.
The Embryology of Heterodontus japonicus 699
On the basis of the mode of suspension of the jaws, it appears impossible to make
a clear-cut distinction between the families Hybodontidae and Cestraciontidae as consti
tuted by Woodward (in Zittel, 1932). Some genera of the Hybodontidae (e.g., Orodus)
are known only by their teeth, or by their teeth and dorsal spines. Where genera are
represented by fairly complete skeletons (e.g., as in Hybodus), there is apparently some
lack of uniformity in the method of jaw suspension. Nevertheless Woodward (1921)
generalized as follows: “The Hybodonts. . . are especially interesting because, while
their dentition and their general appearance resemble those of the existing Cestraciont-
idae, their skull is very different and more closely agrees with that of the Notidanidae”.
It is possible that the word skull, as used here, means cranium, as it seems to do in
several places in Woodward’s writings.
The terms autostylic, hyostylic and amphistylic were introduced by Huxley (1876)
to designate three types of skull and of suspension of the first visceral arch—the mandibu-
lar arch, or the jaws. We are here concerned only with the second and third types as
they occur in sharks. In both, the palatoquadrate cartilage (constituting the framework of
the upper jaw) is quite distinct from the chondrocranium. The palatoquadrate is, at
most, in contact with the cranium only by articular surfaces, and connected with it by
ligaments. In front, the palatoquadrate is often loosely connected with the lateral
ethmoid (preorbital) region of the skull by way of a palatobasal or ethmoid process (of the
palatoquadrate), but this type of connection apparently has little or nothing to do with
the classification under consideration. In most sharks, the dorsal element of the hyoid
arch, called the hyomandibular cartilage, attains a large size, gains an attachment to the
auditory capsule, and becomes the chief apparatus for suspending the palatoquadrate from
the cranium. This type of suspension is called hyostylic, and is exemplified by the skull of
Scyllium (Text-figure 32). In the hyostylic skull the upper jaw is held somewhat away
from the cranium, and retains a considerable degree of mobility. In the amphistylic
skull, according to Huxley, the palatoquadrate cartilage is wholly, or almost wholly,
suspended by its own ligaments; the hyomandibular is small and contributes but little to
its support. Some authors (e.g., Goodrich, 1909, p. 95) have interpreted, or modified,
this definition to require that, in the typical amphistylic skull, the quadrate region of the
upper jaw must have a postorbital articulation with the auditory capsule in addition to
being connected with it by the hyomandibular: as in Heptanchus (Goodrich, 1909, Fig.
59a);a typical Acanthodian (Goodrich, 1909, Fig. 159);and in Hybodus hauffianus accord-
ing to Jaekel (my Text-figure 28).
It will suffice here to attempt a comparison between the skulls of Heterodontus and
Hybodus, with special reference to the manner in which the jaws are attached to the
cranium. The skull of Heterodontus (Text-figure 33) is usually classed as hyostylic,
though it does not conform closely to this type. One should examine also the more
elaborate figures of the skull of Heterodontus phillipi by Huxley (1876, Fig. 8) and that of
H. francisci by Daniel (1915, Fig. 6, pl. IV). In both figures the cranium is more closely
molded on the palatoquadrate cartilages (upper jaws) than is represented in Goodrich’s
700 Bashford Dean Memorial Volume
figure (my Text-figure 33). According to Huxley, the hyomandibular is of moderate
size; it articulates with a process on the underside of the auditory capsule and supports
the posterior end of the palatoquadrate, with which it is connected by a strong ligament-
ous capsule. The huge palatoquadrate is connected with the cranium in the preorbital
region by a broad joint (ethmoidal articulation) and in the orbital region by fibrous tissue.
The postorbital region of the cranium of Heterodontus appears short, and the preorbital
region long, as compared with most sharks. The cranium as a whole is much longer than
the jaws, which appear as if thrust forward. Anteriorly the upper jaw extends almost or
quite as far as the snout, but posteriorly it does not reach the auditory capsule. Thus the
lower end of the hyomandibular cartilage is pulled forward.
In sharks of the genus Hybodus, according to Woodward (1916), the pterygoquadrate
(palatoquadrate) is not articulated with the preorbital region of the cranium (as it is in
Heterodontus). In Hybodus hauffianus, according to Jaekel (1906), the suspension of the
jaws is amphistylic (my Text-figure 28, page 695). The skull of Hybodus dubrisiensis, as
described by Woodward (1886) is even more typically amphistylic, resembling that of
Heptanchus. Woodward's figure shows the palatoquadrate with a small but definite
facet in position for a postorbital articulation with the cranium; the hyomandibular is
slender, but evidently gives some support to the jaws. But in Hybodus basanus, as
described by Woodward (1916), there is no articulation between the palatoquadrate
Text-figure 32. Text-figure 33.
Incomplete skulls of Scyllium and Heterodontus, illustrating methods of suspension of the jaws.
Textfigure 32. The skull of Scyllium, illustrating the hyostylic method of suspension of the jaws.
a., auditory capsule; ch., ceratohyal cartilage; cr., cranium; ep., ethmoid process; h., hyomandibular branch of facial nerve; hm., hyoman-
dibular cartilage; 1., labial cartilage; mk., Meckel’s cartilage; na., nasal capsule; g., quadrate region of the palatoquadrate cartilage;
r., Tostral process; sp., spiracle.
After Goodrich, 1909, Fig. 59c.
Text-figure 33. Cranium, jaws and hyoid arch of the Port Jackson shark, Heterodontus phillipi.
a., auditory capsule; ch., ceratohyoid; ea., ethmoid articulation; hm., hyomandibular; 1., labial cartilage; mk., Meckel’s cartilage;
na., nasal capsule; nc., nasal cartilage; g., quadrate region of the palatoquadrate; pc., prespiracular cartilage. A dotted ring behind
the prespiracular cartilage indicates the position of the spiracle.
After Goodrich, 1909, Fig. 58a.
The Embryology of Heterodontus japonicus 701
and the cranium. In the skull of Hybodus basanus (my Text-figure 34), the cranium is
rather short, with a relatively large orbit and with short postorbital and rostral regions.
The jaws, which are relatively large and massive, are longer than the cranium, so that the
hyomandibular suspensorium extends backward, while the upper jaw extends forward as
far as the end of the snout. The rami of the mandible, though deep and massive behind,
rapidly taper forward and meet in a com-
paratively feeble symphysis which does not
extend so far forward as the front of the
Text-figure 34.
Restoration of the skull of Hybodus basanus
Egerton, a little less than one-half natural size.
The deeply shaded portion is the orbit.
cr., cranium; hy., hyomandibular; 1., one of the labial cartilages;
m., lower jaw or mandible; q., quadrate region of the pal-
atoquadrate. The lettering does not appear on the original.
After Woodward, 1916, Fig. 3s.
upper jaw. The palatoquadrate is weak and
depressed at its anterior end, but deepens
rapidly backward. According to Woodward,
it can scarcely have articulated with the postorbital prominence of the cranium.
According to Huxley (1876) the skull of Heterodontus is the link that connects the
primitive amphistylic skull with the ordinary selachian skull, which is hyostylic. Like-
wise, Goodrich (1909) wrote: “. . . it is well established that Hybodus and Synechodus had
typical amphistylic skulls, with the palatoquadrate and hyomandibular as in the Notidani-
dae and other primitive Elasmobranchs.” This view accords with Woodward's observa-
tion (1886) that the skull of Hybodus dubrisiensis is typically amphistylic, and with
Jaekel’s interpretation of the skull of Hybodus hauffianus (my Text-figure 28); but it
does not harmonize with Woodward’s later statement (1916) that the pterygoquadrate
(palatoquadrate) of Hybodus basanus “can scarcely have articulated with the postorbital
prominence of the cranium”. It seems remarkable that species of the same genus should
differ ina manner so important; but if the skull of Hybodus basanus really does lack a post-
orbital articulation with the cranium, then it is hyostylic and therefore more like the skull
of Heterodontus. By the same token, if such divergences can exist within a single genus of
Hybodonts, how trivial become the differences between the skulls of any species of the
Mesozoic Hybodus and the present-day Heterodontus! In view of the well-known difh-
culties attending the restoration of the fossil vertebrate remains to life-like attitudes, one
suspects that there is a flaw in the data somewhere; but, considering the long lapse of
time, the evolution of the skull of Heterodontus from that of any Hybodont does not seem
impossible.
702 Bashford Dean Memorial Volume
It is apparent that paleontologists have experienced considerable difficulty in
disentangling the Cestraciontidae from the Hybodontidae. The two families have, at
least once, been lumped together, and authors have seldom agreed on the criteria by means
of which they should be divided. Wherever the line has been drawn, the distinction
seems more or less arbitrary: the differences between the families seem no more impressive
than the differences between genera within at least one of the families. These facts
cannot be wholly explained on the ground of difficulty in reading the paleontological
record: for nearly complete skeletons belonging to several different genera have been
obtained. The only adequate explanation is that there exists a close genetic relationship
between the families. With respect to families other than the Hybodontidae, the Het-
erodontidae occupy a relatively isolated position. Woodward (1921) states that the
Hybodonts are a generalized group from which several later families appear to have
risen. They were the dominant sharks of the Jurassic and Early Cretaceous Periods. To
the present writer it seems not only possible but highly probable that the Mesozoic
Hybodus, or some Hybodont closely related to it, is the direct ancestor of Heterodontus.
After this glimpse into the past, we return to the study of living Heterodonid sharks.
SEXUAL DIMORPHISM AND THE REPRODUCTIVE ORGANS
Concerning the Port Jackson Shark, Heterodontus phillipi, Maclay and Macleay
(1879) state that the two sexes scarcely differ in size and marking. With the aid of special
drawings, they describe the intromittent organs (myxopterygia or ““claspers”) of the male
H. phillipi. More recently, the claspers of three species of Heterodontus (phillipi, japonicus
and galeatus) have been described and figured by LeighSharpe (1922 and 1926). Some
marked specific differences in this organ are noted.
According to Dean’s notes, Heterodontus japonicus shows marked sexual dimorphism.
The female is larger than the male, heavier in body and somewhat different in proportions.
Dean states that the female, when full-grown, measures about 1200 mm. (47 inches) in
total length: the male, about 1000 mm. (39 inches). There is little difference in color,
though Dean at one time believed that the males could invariably be distinguished, in the
well of a fishing boat, by a darker and richer tone.
Since I have no adult female specimen of H. japonicus available for dissection, it is
a satisfaction to be able to record the results of my examination of the reproductive organs
of the larger female specimen of H. francisci belonging to the American Museum of
Natural History. This shark is 705 mm. (27.7 inches) long, and is fully adult. The oviducts
of both sides of the body are well developed, with especially large, thick-walled shell
glands. Evidently both oviducts are functional. As in the adults of most sharks, the
two oviducts have a common abdominal aperture. In decided contrast to the oviducts,
the ovaries of the two sides of the body are very unequally developed.
On the right side, the large ovary contains eggs in various stages of development. Of
these, the two largest measure about 35 mm. in diameter, the next largest one about
The Embryology of Heterodontus japonicus 703
30mm. The smaller ovocytes remaining in the ovary are all 12 mm. or less in diameter.
It is not known whether H. francisci, like H. japonicus, matures and deposits its eggs in
pairs; but it is possible that this may be the case, for the ovary under consideration had
been injured in making a large incision in the body wall to admit the preserving fluid.
From this opening, part of the ovary protruded, and one large mutilated follicle contained
only a few fragments of an egg. The mesentery supporting the ovary extends posteriorly
almost to the rectal gland. Throughout much of its extent it is thickened by what
appears to be a posterior sterile portion of the ovary. This is probably the “epigonal
organ” of certain sharks, which extends from the ovary along the dorsal body wall
posteriorly to where it joins the mesentery of the rectal gland (Daniel, 1922, p. 316). On
the left side of the body the ovary is rudimentary—so slender and smooth that it could
scarcely be recognized as an ovary except by position and relations. The epigonal organ
is much larger—dquite as large as the one on the right side. The right and left epigonal
organs differ in shape: the one on the right is broader and thicker anteriorly, tapering
posteriorly; the reverse is true of the one on the left. Ovary and epigonal organ of the
left side (like those on the right) are continuous structures, supported by a single con-
tinuous mesentery.
Among Dean’s records I find a drawing of a dissection showing the reproductive
organs of an adult female Heterodontus japonicus. This drawing (my Text-figure 35) is
not labelled, nor is it described in Dean’s notes, and in the absence of the dissection some
features are obscure. In the mid-line near the top of the figure, one readily notes the
common abdominal opening of the oviducts. On the extreme right side of the figure
(left side of the fish) the oviduct with its three divisions— oviduct proper, shell gland and
uterine portion—are easily identified. Halfway between the oviduct and the mid-line of
the body there is an elongated object of which the anterior portion is a rudimentary
ovary, the posterior larger portion the epigonal organ. This rudimentary ovary is not so
slender as the corresponding ovary of H. francisci described in the preceding paragraph.
The rectal gland is visible in the mid-line near the lower end of the abdominal cavity. On
the left side of the figure (right side of the fish) the oviduct, excepting the posterior end
of its uterine portion, is obscured by other organs. Apparently the intestine, which
together with the stomach occupies a large part of the left side of the figure, has been
transected at its posterior end to aid in turning it aside. The relations of the mesenteries
on this side of the fish are obscure. It is probable that the epigonal organ of the right side
of the fish is concealed by the stomach and intestines. It is unfortunate that these organs
were not removed. The right ovary is conspicuous in the upper left part of the figure, and
this organ deserves special consideration. .
The right ovary shown in Text-figure 35 contains a number of large eggs, of which
two are larger than the others. In one fish, Dean observed two ovarian eggs which were
almost ripe, showing large “stigmata” (orange spots or germinal discs?). The other eggs
of the same ovary were smaller. Nothing is written concerning the condition of the
eggs, if any, in the other ovary. It is not known whether the fish whose ovarian eggs are
704 Bashford Dean Memorial Volume
Text-figure 35.
Dissection showing the reproductive organs of an adult female Heterodontus japonicus.
Note that the right ovary contains two eggs much larger than the others.
From a drawing left by Bashford Dean. The paper on which this drawing was made is much darkened
by age, hence the drawing is not so clear as it must have been originally.
The Embryology of Heterodontus japonicus 705
thus described is the one represented in Text-figure 35. Dean states that though several
gravid sharks yielded each but a single encapsuled egg, in each case the condition of the
“opposite” ovary indicated that another egg had already been laid. These observations
support the data recorded in the section on “Egg-laying Habits”, and indicate that two
eggs are laid at about the same time. We also infer that occasionally both ovaries are
functional at the same time. From Text-figure 35 it appears that the “uteri” of both
sides are well developed.
THE EGG CAPSULE: ITS STRUCTURE AND FUNCTIONS
The earliest published drawings of the egg capsule of Heterodontus phillipi are
those of Duméril (1865), reproduced as my Text-figures 36a and 368. These drawings
have been extensively copied, but Waite (1896) states that they are not very good, being
doubtless drawn from dry and distorted specimens. The frayed condition at the apices of
the two spiral appendages is an artifact. McCoy (1890) contributed a drawing that
differs from Dumeril’s in that the apices of the two spiral appendages are blunt and are
not frayed. McCoy states that these
“eggs” (capsules) are conical in shape,
about six inches long, and surrounded with
two broad keels extending spirally and
obliquely round the egg from one end to
the other, like six turns of a broad screw;
the substance is of a tough, dark-brown,
horny appearance.
A suggestion as to the advantage of
the peculiar form of the Heterodontid egg
is offered by Allen (1892) as follows:
That well-known frequenter of Aus-
tralian harbours, the Port Jackson Shark,
lays a pear-shaped egg, with a sort of spiral
staircase of leathery ridges winding around
it outside, Chinese pagoda-wise, so that
even if you bite it (I speak in the person of
a predaceous fish) it eludes your teeth, and
goes dodging off screw-fashion into the
water beyond. There’s no getting at this
evasive body anywhere; when you think Text-figure 36.
you have it, it wriggles away sideways and Egg case of the Port Jackson shark, Heterodontus
refuses to give any hold for jaws or palate. _phillipi: A, entire specimen; B, egg case with interior
In fact, a more slippery or guilefulegg was exposed. According to Duméril the egg case is about
never yet devised by nature’s unconscious 130 mm. (5.1 inches) long.
ingenuity. After Duméril, 1865, Atlas, Figs. 2 and 3, pl. 8.
706 Bashford Dean Memorial Volume
Text figure 37.
ules of Heterodontus phillipi and H. galeatus: A, egg case of H. phillipi; B, egg case of
Fgg cap
nm
of H. phillipi is about six inches (152 mm.) long; that of H. galeatus 4.5 inches (114 mm.) long—
presumably without the tendrils.
After Waite, 1896, pl. 12.
The only adequate account of the egg capsules of Heterodontus phillipi is that of
Waite (1896), who also described the egg capsules of H. galeatus. His drawings of the
egg capsules of both species are reproduced as my Text-figure 37. Because of their
unique value, Waite’s descriptions are here quoted in full.
The egg cases of both species [phillipi and galeatus] have the following points in com-
mon: All parts are composed of a flexible horn-like substance of brown color. The body
consists of a chamber, shaped like a pear; the coronal portion is compressed into a cervix
through which the young shark eventually escapes. From each side of the cervix, and integral-
ly connected with it, arises a ribbon exactly resembling a strip of kelp. These ribbons are
attached basally, their free edges turned towards the cervix and deflected considerably from
the body. They pass round alternately and obliquely, and form the thread of a righthanded
double screw, together making five or six turns to the base [smaller end of the capsule]. These
ribbons originate [with] about half the width they quickly attain, and continue their course
of even breadth, again narrowing on approaching the base. The interior, as shown by
a section [Text-figure 37s] is wide and capacious; the fissure does not proceed to the base as
generally portrayed, but terminates some distance short of it; the inside is marked with
oblique striae corresponding to the direction of the spirals, and resembling the lines inside
a vessel turned upon a potter’s wheel.
The principal differences between the egg cases of the two species may be recounted
thus: Cestracion [Heterodontus] phillipi [Text-figures 374 and 37s]: Of larger size; about
The Embryology of Heterodontus japonicus 707
six inches in length. The spirals are very broad and, in part, hide the body when viewed
laterally; at the base they narrow quickly and terminate bluntly, and are not produced into
tendrils. Beach-worn examples generally have the terminations more or less frayed.
Cestracion [Heterodontus] galeatus [Text-figure 37c]: Of smaller size; about four inches
anda halfin length. The spirals are not very broad, and in no part hide the body completely;
basally they become narrow and are produced into long flattened tendrils. In the most
perfect specimen examined, each tendril is 90 inches in length, and tapers to the slenderest
thread, becoming tangled and knotted like a skein of silk. They are, however, very tough,
and may be unravelled without fear of breaking. One of the tendrils terminates in a thick
ened tag (shown in the figure) which, although doubtless an individual peculiarity, indicates
that the tendrils are entire.
Further, Waite calls attention to the fact that the appendages, with which the egg
capsules of sharks are furnished, serve to moor them in some suitable situation, otherwise
they would be likely to be knocked about to the detriment of the contained embryo, or
might even be washed ashore where their destruction would be certain. The spiral
appendages of Heterodontus phillipi are no exception to the rule; the elastic flanges permit
the egg to be forced further into a fissure, whence extraction is resisted by the free edges
of the ribbon catching against the rocks. Although, in a lesser degree, the egg case of
H. galeatus possesses these spirals, they do not appear to have the same use; for attach-
ment is here effected by the entanglement of the tendrils among seaweed.
The egg capsule of H. francisci is figured by Daniel (1934, also in earlier editions).
His figure is reproduced here as my Text-figure 38. This
capsule lacks tendrils and bears a general resemblance
to the egg capsule of H. phillipi; but it is more slender.
Text-figure 38.
Egg capsule of Heterodontus
francisci.
After Daniel, 1922, Fig. 254, p. 318.
Text-figure 39.
An egg case of Heterodontus
japonicus with an opening
cut to show the young em-
bryo within. The cleft in
the upper left-hand portion
of the figure follows the line
of the respiratory groove.
After Doflein, 1906, p. 209.
708 Bashford Dean Memorial Volume
The spiral flanges are narrow at the broader end of the capsule, and widen as they
approach the narrower end.
Barnhart (1932) states that the egg case of H. francisci is about 120 mm. (4.7 inches)
long, and 50 mm. (2 inches) wide at its largest diameter, with two wide flaps running
spirally from end to end (as in his Fig.1). The size varies, depending probably on the
age of the parent. I haveno definite information concerning the egg cases of H. zebra
and H. quoyi.
Before entering upon a somewhat detailed account of the structure and functions of
the egg capsule of Heterodontus japonicus, it seems desirable to examine some general
features of this capsule as a basis for comparisons with the other species already con-
sidered. Egg capsules of H. japonicus are illustrated in Text-figures 39 and 59 (page 752),
also in Figures 76 to 78, plate VII. These capsules appear to be stout-bodied, like those of
H. phillipi and H. galeatus—not slender like those of H. francisci. The width of the spiral
flanges is less than in H. phillipi, greater than in H. galeatus, and approximately the same
as in H. francisci. In the capsules of H. japonicus the two spiral flanges make comparative-
ly few turns about the body of the capsule: each flange encircles it from one and one-half
to two times. In the capsules of the other species considered, there are nearly twice as
many turns of the spiral flanges. In other words, in the capsule of H. japonicus the
spirals formed by the flanges are unusually loose. Since in this species the flanges are
only moderately wide, it follows that an unusually large amount of the surface of the
body of the capsule is exposed.
The primary function of an egg capsule is of course protective, but provision must
be made for the aeration of the embryo and for its eventual hatching. The gross structure
of the egg capsule of Heterodontus japonicus, and its role in respiration and hatching, are
described in Dean’s notes on which the following account is based.
The capsule of H. japonicus (Figures 76 to 78, pl. VII,) varies considerably in size:
in length from 120 to 180 mm. (4.7 to 7 inches), and in weight from 145 to 238 grams,
including yolk and embryo. It is somewhat conical in shape, drawn toa point at one end
(“lower’”’, distal or “‘vegetal’’) but to a “‘chisel-like” edge at the other (“upper”’, proximal
or “animal’’). It is provided with two marginal bands which encircle the capsule spirally
somewhat as the “thread” surrounds a screw. These bands arise at the sides of the upper
or broad end of the capsule, and are homologous with the marginal bands which occur in
the egg capsules of many sharks and chimaeroids. But instead of passing straight down-
ward, they wind about the capsule two and a half times (according to Dean’s notes)
until they terminate with short processes at the lower end. Here the spiral bands are
wider and are more nearly transverse. The freshly deposited capsule is dark bottle-green
in color, as shown for the first time in Dean’s drawings (Figures 76 to 78, pl. VII). Later
the capsules become paler, brownish or sometimes ochreous. Altogether they resemble
certain large cysted brown sea-weeds, but whether this resemblance is a protective one
is not known.
The Embryology of Heterodontus japonicus 709
While the embryo of H. japonicus is developing, the capsule undergoes steady
deterioration, as in Chimaera (Dean, 1906) and in other elasmobranchs. The substance of
the capsule becomes thinner, more “tense” and fragile. An arrangement is also developed
which enables the young fish to carry on respiration. At either side of the upper or
larger end of the capsule, near the line of junction of each marginal band, there is a deep
infolding in the wall (as indicated by the arrow in Figure 76, plate VII). Later, by a process
of weathering, this respiratory groove opens and widens asa slit (Text-figure 59, page 752).
(A respiratory slit of this kind in the eggs of elasmobranchs appears first to have been
mentioned, though hardly described, by Home, 1810, page 213). In addition, similar
respiratory slits appear at the “lower” or more pointed end of the capsule.
The upper slits in the egg capsule of H. japonicus play an active role in the process
of hatching, which is described by Dean as follows:
By a continuation of the process of weathering, the upper slit comes to open not only in
its lower portion (i.e., in the direction of the contained egg) but in an extended line along
the upper and median margin [of capsule]. By this process the entire chisel-like rim of the
capsule finally weathers open, and its sides separate, leaving a slit between. This follows
the absorption of the hard wedge of albumen which has from the beginning blocked up the
large end of the capsule. Old capsules, it was observed, are “tense”, and hatching occurs
with a rapidity which reminds one of the dehiscence of certain seed pods. The sides of the
terminal aperture open and shut in a twinkling, and one is given the impression that the
young fish is shot out of the capsule. There is a writhing on the part of the imprisoned fish,
and it emerges with a rapidity which quite disconcerts the observer if, as in my own experience,
he happens to be holding the egg capsule in his hand. [For further details, see page 753].
Among the capsules which passed through Dean’s hands, there were several which
were newly deposited and perfect except that none contained an egg. Such empty
capsules are called “wind eggs”. Externally, these capsules were quite indistinguishable
from the others, except by their lighter weight. Dean assumed that they resulted from
unilateral ovulation, during which the oviduct of the side opposite to the gravid one was
stimulated to produce a capsule.
HABITS OF HETERODONTUS
In this section, and in those that follow, we are concerned primarily with the
Japanese species, Heterodontus japonicus; but reference will be made to other species
wherever information is available.
HABITAT AND GENERAL HABITS
There is a curious lack of information concerning the depths at which adults of some
species of Heterodontus have been taken, though depths at which the eggs of one of
these species have been found are recorded in a later section of this article. Osburn and
Nichols (1916) record the capture of a specimen of Gyropleurodus (Heterodontus) francisci
8 inches long, dredged from 13 fathoms of water, in Magdalena Bay, Lower California.
710 Bashford Dean Memorial Volume
Regarding the same species, Barnhart (1932) writes that, while many of these sharks have
been taken in shallow water, there are several instances of large numbers being taken at
depths of over 500 feet by rock-cod fishermen. He further states that this species migrates
from shallow to deep water and from deep to shallow water at certain times of the year.
Whitley (1940) states that Heterodontus phillipi is found in littoral waters to a depth
of 94 fathoms.
According to Dean’s notes, Heterodontus japonicus (called Nekosamé by the natives
at Misaki) occurs in moderately shallow water, roughly between 3 and 20 fathoms. It
frequents places where the sea bottom is covered with rock fragments or sea-weeds.
Concerning the habits of Heterodontus, other than feeding and spawning habits, our
information is very meager. Of H. phillipi, the Port Jackson Shark, Maclay and Macleay
(1879) write that the adults are very tenacious of life, but no data are given to support
this statement. For H. japonicus it is possible to quote directly from Dean’s manuscript
as follows:
Cestracion [Heterodontus japonicus] is deliberate in its movements: it swims slowly,
and changes its direction readily. Its great pectoral fins are inactive; in fact for a form so well
provided with large fins it seems to make surprisingly little use of them. Nor is it alert.
Indeed, the divers took by hand the greater number of specimens which were brought to me,
although it may well be that the fish, being about to deposit eggs, were less attentive to
externals than under usual conditions. The divers report that ““Nekosamé”’ stays close to the
bottom and spends its time “nosing” among rock fragments and seaweeds. When disturbed it
swims off near the bottom, and not over the heads of the divers as many fishes do.
FOOD AND FEEDING HABITS
Concerning the Port Jackson Shark, Heterodontus phillipi, Maclay and Macleay
(1879) wrote that its stomach is generally well-filled with fragments of shells, but these are
not so well comminuted as might be expected from the character of the teeth; and that
the “bowels” are often well charged with cestode worms. McCoy (1890) states that
this shark is common in Hobson Bay (Victoria), and that the stomach is filled with
fragments of shells. Some interesting information regarding the feeding habits of the
Port Jackson shark is furnished by Saville-Kent (1897, pp. 192-193), as follows:
- Oysters are the favorite food of this shark [Heterodontus phillipi], and in consequence
of its predilection for this bivalve, it has proved a formidable enemy to oyster growers in
both Tasmania and on the mainland seaboard. At Spring Bay, in the former island colony,
the writer found it even necessary to fence round certain of the Government Oyster Re-
serves with closely matted brushwood in order to protect the oyster stock laid down, from
this shark’s depredations. In some localities, Cestracion [Heterodontus] feeds almost ex-
clusively upon Sea Urchins or Echini, the sharp spines of which have apparently no other
effect than the pleasant titillation of its palate. The proof of the extent to which this piquant
food is favored by this shark is afforded by the fact that the entire pavement of teeth of
captured specimens are not infrequently permanently stained a deep purple, through constant
indulgence in a dietary of the commoner purple urchin.
The Embryology of Heterodontus japonicus 711
Maclay and Macleay (1879) state that Echini (Sea Urchins) form the chief food of
Heterodontus galeatus and probably of all the genus. The strong dorsal spines and the
prominent supraorbital ridges of these sharks enable them to force their way under rocks
and stones in pursuit of their prey. A fine specimen of H. galeatus in the Macleay
Museum had the dorsal spines worn down to half their proper length, evidently as a result
of scraping against rocks, and its “viscera” were full of finely triturated Echinus tests.
My only information regarding the food and feeding habits of the Japanese Bullhead
Shark is derived from Dean’s manuscript, from which I quote the following:
It [Heterodontus japonicus] is a
bottom feeder, and is known to have
a varied diet: crustaceans, mollusks, fish
and sea urchins. With its formidable
dentition it crushes mollusks of consid-
erable size, and its well-worn grinding
teeth show that the crushing of shells
is a frequent habit. At first sight the
mouth appears extremely small, and one
gets the impression from the narrow
ends of the jaws which are exposed that
the fish is a “nibbler’’, and cannot open
its mouth widely. The photograph,
however (Text-figure 40) shows how
completely the shark may open its
mouth; and the captive fish is apt to
offer many demonstrations of this habit.
The jaws in such cases will sometimes
be snapped together noisily, indicating
great muscular leverage. In the case
figured, the fish was an old one and its
mouth was by no means in good order.
On either side of the large teeth were Tse ame 20,
tufts of sertularian hydroids; also there
View of the wide-open mouth of a new-caught Hetero-
were half a dozen leechesintheneighbor- dontus, presumably japonicus. Note the large grinding
hood, some specimens measuring about teeth in the posterior part of the roof of the mouth.
2!5 inches in length. From a photograph taken by Bashford Dean at Misaki, Japan.
BREEDING SEASON
Concerning the Port Jackson Shark, Heterodontus phillipi, Maclay and Macleay
(1879) state that, if the accounts of the fishermen are to be believed, it is very slow of
reproduction—the females never having more than two eggs at a time and only one
brood a year. McCoy (1890) states that Cestracion (Heterodontus) phillipi never lays
more than two eggs at a time, and only once a year. He does not say how or where he
obtained his information. In view of the results obtained by Dean through examination of
2 Bashford Dean Memorial Volume
the ovaries of H. japonicus, the statement that the Port Jackson Shark spawns but
once a year cannot be accepted without further evidence.
Waite (1896) writes that living eggs of Port Jackson Sharks Goane both H.
phillipi and H. galeatus) are most abundant in spring (August and September) but are
found also throughout the summer. The empty egg cases may be found washed up on
beaches at any time of the year, especially after stormy weather. At Jervis Bay, New
South Wales, Haswell (1898) collected eggs of H. phillipi in blastula and gastrula stages
during September (a spring month in the southern hemisphere). It appears that he found
eggs in these stages in considerable numbers. He does not mention any later stages
collected during September. Whitley (1940) states that he has observed developing
embryos of H. phillipi in December, and young hatching in May.
Regarding the eggs of H. francisci, Barnhart (1932) states that material collected
tends to show that several eggs are spawned during the year.
In the region of Misaki, according to Dean’s notes, spawning of Heterodontus
japonicus takes place throughout the entire year but the especial spawning season is
evidently the month of March. The divers brought in the maximum number of eggs
during April and May, and most of these were in stages which Dean estimated to be
a month or six weeks old. Throughout June, eggs in early stages of development were
brought in occasionally; throughout July, early stages were still more uncommon, perhaps
one in twenty; and later in the season, early embryos were found but rarely. Supple-
mentary evidence in regard to the breeding season was obtained by examining the ovaries.
Judging from the condition of the ovarian eggs, Dean concluded that H. japonicus spawns
a number of times during the “season”, probably from six to twelve times, and that two
eggs are matured at about the same time. During the spring months the eggs are evidently
deposited at short intervals. This is deduced from the presence of almost ripe ovarian
eggs in Japanese Bullhead Sharks from which encapsuled eggs were obtained. Further
data bearing on the breeding season are given in the section on “Rate of Embryonic
Development”.
EGG LAYING HABITS; THE NESTS
Waite (1896) wrote that the eggs of Cestracion (Heterodontus) phillipi were found in
moderately shallow water, wedged in among rocks. Whether they were actually dropped
into the crevices he did not know, but he thought it more probable that they were
deposited on the sand at the bases of the rocks, into the fissures of which they were after-
ward swept by the tide. They were so jammed, larger end outward, that they could
only be removed either by turning them around and withdrawing the small end first, or by
actually unscrewing them; both forces being most unlikely to occur under natural con-
ditions. When empty they are somewhat more pliable, which may account for the empty
capsules being loosened and cast ashore. Ina later publication (1899) Waite wrote that
H. phillipi was common in Jervis Bay (New South Wales) which was for these fishes
a favorite breeding resort. Here, empty egg cases could be found in large numbers washed
The Embryology of Heterodontus japonicus 713
ashore or wedged in among rocks; here also, in 20 fathoms of water and under, living eggs
might be freely obtained.
Haswell (1898) likewise collected capsules containing living eggs of H. phillipi in
Jervis Bay, New South Wales. He states that he found many of these at low tide,
sticking in the crevices of the rocks, firmly wedged in by means of the spiral flange which
forms such a remarkable feature of the egg shell.
So little is known about the spawning habits of H. galeatus that the following account
of their spawning grounds, quoted from Waite (1896), may be of interest:
Although most rare upon the beaches, the eggs of C. [Heterodontus] galeatus prove to be
not uncommon when searched for in their native habitat. Through the kindness of Messrs
Darley and Grimshaw, I recently had the pleasure of searching for them 50 feet below the
surface. Although not successful in obtaining specimens, I got an excellent idea of the
general situation. In places, immense masses of brown seaweed grow to the height of two
or three feet so densely that scores of eggs may be securely concealed among them, protected
by their likeness to seaweed in color and texture. Mr. Cameron, the diver who kindly took
me in charge, told me that he always finds the eggs in the weed, so attached by their long
tendrils [Text-figure 37c] that it is scarcely possible to secure them whole, without cutting
the seaweed. In deep water they are freer from the violent disturbances, tending to detach
them, to which the eggs of the more common species (H. phillipi) are subject
Barnhart (1932) writes that eggs of H. francisci are frequently found wedged between
or under rocks in the extreme low-tide zone.
In his notes Dean states that one can usually determine when a Heterodontid shark
is gravid by noting the greater abdominal girth. Also, a digital examination can readily
be made. In order to understand the process of egg laying in the Japanese Bullhead
Shark, one should be familiar with the external form of the egg capsule which is described
in a previous section of this article.
Heterodontus japonicus deposits two eggs at about the same time. In numerous
instances encapsuled eggs were brought to the station (at Misaki) in pairs, and in the
same stage of development. It was therefore assumed that they had been deposited in
pairs. This assumption was verified on two occasions, when pairs of encapsuled eggs
were taken directly from the fish. Evidence that two eggs mature at about the same
time has been given in the section on the reproductive organs.
Data as to the mode of depositing the egg are scanty. The fish is apt to fold its
pelvic fins around the cloacal region, and one must bend the fins aside in order to see if
a capsule is protruding. In one instance, a shark brought to the station deposited an egg
within a few hours (Text-figures 414 to 41D). When the fish was first examined (Text-
figure 414) no trace of a capsule could be seen between the pelvic fins. An hour or two
later, the smaller end of the capsule protruded slightly (Text-figure 418). Within an
hour, a second turn of the capsule’s lateral frill or spiral lamina could be seen (Text-figure
41c) and in less than an hour later there appeared Text-figure 41p) the third turn of the
frill. At this time the egg slipped out, and Dean noted that in the final rapid phase of
714 Bashford Dean Memorial Volume
Text-figure 41.
Ventral view of the pelvic region of a female Heterodontus japonicus showing a series of stages (A to D) in the
process of extrusion of the encapsuled egg. In A, the cloacal region is shown between the pelvic fins, but the
extrusion of the egg has not commenced. In D, the dotted lines represent portions of the egg case still within
the body of the mother.
From drawing left by Bashford Dean.
extrusion the capsule rotated about its long axis as though it had been unscrewed.
Evidently this was not the only occasion when Dean saw an egg protruding from the
cloacal aperture of one of these sharks, for on the margin of his drawing reproduced as
my Text-figure 41p there was found a penciled note in Dean’s handwriting: “Sometimes
4 ridges show”.
Dean thought that, in the case just described, the final extrusion of the capsule was
hastened by unskillful handling of the fish. But he notes that there are several considera-
tions indicating that the sudden extrusion of the capsule, which he observed, may have
been like the normal process of deposition. The capsule at this stage is very slimy. The
shark exercises a voluntary control over the sphincters of the oviducal apertures. It can
tighten or loosen its hold on the capsule, and it may even envelop the entire cloacal region
with the bases of the pelvic fins. The very suddenness of the process may have a distinct
advantage to the fish, for by it the capsule, on account of its peculiar form, is caused to
rotate—a motion which would obviously project it downward and backward in a straight
line, making it less subject to deflection by water currents.
Ecces Founp 1n Nests.—Of special interest is Dean’s account of the occurrence
of the eggs of Heterodontus japonicus in “nests” on the sea bottom:
It is well known by the fishermen that the eggs of “Nekosamé” are found among rock
fragments. On sandy bottom and in weedy reaches they rarely occur. The professional divers
(with suits) whom I employed to search for these eggs in the neighborhood of Misaki examined
carefully various kinds of bottom in water from three to eight fathoms, but without success,
for at that time we had not discovered where the eggs are usually located. For this discovery
I was indebted to the fishermen who dive for Haliotis, and from them I learned that the eggs
of Cestracion (Heterodontus) occur in “nests”. An instance of their mode of occurrence may
be cited.
The Embryology of Heterodontus japonicus 715
A “nest” was discovered October 4, 1905, in the channel off the fishing town of Miura-
Misaki behind the island Jogashima, at a depth of 28 feet. It contained 15 eggs in various
stages of development. The bottom of the nest was of seaweed, its sides were formed by
irregular rock masses, some of large size, and the nest was largely concealed by several flat
stones which the divers removed only with difficulty. (It appeared fortunately that this
particular spot was rich in Haliotis and was being inspected with great care). The eggs were
shown to be arranged in a space about six feet long, the greater number of them lying together
closely embedded in the seaweed, “‘four out of five” of them being wedged in, with the little
end of the capsule downward. I visited the spot and it may be worth while to picture
a restoration of this nest (Text-figure 42) as near as I could make it out without diving, relying
upon the fisherman’s reconstruction.
From the preceding account, it appears that there is similarity in the egg capsules
and in the spawning habits of Heterodontus phillipi and H. japonicus. In both species,
\
Sup
Mh...
I
A
\\ NK
\, NNR
Text-figure 42.
Reconstruction of a typical “nest” of Heterodontus japonicus found at the bottom of the Sagami Sea at a depth
of 28 feet. The nest was surrounded by large rock fragments. Some encapsuled eggs may be seen entangled
among sea weeds at the bottom of the nest, and other eggs are wedged into crevices in the rocks.
Ny
\Y
From a drawing by Bashford Dean, whose initials appear in the lower right-hand corner.
716 Bashford Dean Memorial Volume
bluntly, without tendrils. These eggs are deposited on the sea bottom among large rock
fragments, or surrounded by rocks. In such situations, some become entangled in sea-
weeds, others wedged into crevices between rocks. The egg capsules of Heterodontus
galeatus are different, in that the spiral appendages are narrower and end in very long and
slender tendrils which become thoroughly entangled among seaweeds. The only records
available indicate that living eggs of these species have been taken at the following depths:
Heterodontus japonicus at 28 feet; H. phillipi at 120 feet or less: and H. galeatus at a depth
of 50 feet. There is no record of any direct observations of the process of egg laying by any
species of Heterodont shark in its natural habitat.
METHOD OF COLLECTING EGGS AND EMBRYOS
The earliest developmental stages of the egg of Heterodontus phillipi figured by
Haswell (1898) were already in late cleavage. These were eggs that had been deposited—
as stated more explicitly in a later article by the same author (Haswell, 1916). In this
later paper, Haswell described some eggs taken from oviducts (“uteri”). Of these, the
two earliest stages were portrayed in a figure which is reproduced as my Text-figure 49a
and 498 (page 731). The other eggs, taken from uteri some weeks later, showed more
advanced stages of cleavage.
As previously stated, the eggs of Heterodontus japonicus were collected at all seasons
of the year. According to Dean’s notes, the greatest numbers of encapsuled eggs were
taken during the month of May. They were gathered in small numbers daily, the
maximum catch being 21, a number as large as 8 or 10 being uncommon. The greatest
number of eggs came from the fishing village of Nagai, between Misaki and Hayama.
The precise method used in collecting the eggs is not only interesting but is of
technical importance. It is well described in Dean’s own words:
In collecting eggs of Cestracion [Heterodontus] divers are indispensable. But these are
fortunately numerous in the neighborhood of Misaki, where they are constantly scrutinizing
the shore rocks for edible mollusks, especially Haliotis. They have thus an excellent training,
for if they can detect these protectively colored limpets, they can observe closely enough to
collect shark eggs; moreover they are in the habit of examining fissures between the rocks,
and they frequently displace stones of considerable size. In general their operations are
usually carried on in water of from 12 to 30 feet, though they sometimes exploit a depth of
40 feet—all this without the use of special suits, the divers usually swimming to the bottom,
remaining under several minutes (2 to 6). They operate usually in pairs, going about in
sampans, each boat provided with a screen, and an hibachi (fire-pot) over which the fishers
crouch during intervals of rest. A familiar sound near the zoological station at Misaki is the
peculiar whistle of the diver as he expands his lungs before going down.
Dean states that the eggs are hardy, and are readily kept alive in floating cages. Thus
the various embryonic stages may be selected from time to time. The stage of development
may be determined with fair precision without the necessity of opening capsules at
random, for the character of the capsule gives a clue to the period of incubation. The
The Embryology of Heterodontus japonicus ale)
capsules with a slimy coating are those recently deposited, and the degree of sliminess
lessens perceptibly during the first days and weeks. The capsule then acquires a smooth
but elastic surface; the spiral band is thick and rubber-like. In later stages the capsule be-
comes rougher in texture, thinner and more brittle; its upper and lower edges become
frayed, and its lateral band is apt to be imperfect. On its surface various foreign growths
appear : bryozoa and barnacles especially.
When capsules were opened and kept in aquaria, the young (still within the capsules)
lived for some time. Early stages were kept alive for several days, especially if well-
covered with albumen; later stages lived for weeks. Death in such cases results ultimately
from invasion of bacteria and infusoria: these attack the yolk, causing it to soften in spots
and finally to break down.
Several times, Dean obtained gravid females; but he never found eggs whose capsules
were in an early stage of formation. The adult Heterodontus japonicus is not often taken.
It rarely is caught in seines, probably because it occurs in regions where rocks are abundant
and where a seine is not likely to be drawn. Even when netted, it is rarely retained, for
it is not marketable (see also pages 688 and 694). Since it was found impracticable to
secure a large supply of spawning fish, the stages of fertilization and beginning cleavage
were not obtained. These stages doubtless occur during the descent of the egg and its
enclosure in the capsule. The earliest embryonic stages studied by Dean were fairly
early (but not the earliest) cleavage stages (Figures 7 and 8, plate I). These were eggs
already in capsules which were practically completed, and were soon to be deposited,
Dean states that the egg is ina blastula stage at the time of deposition.
Heterodontus japonicus, like H. phillipi, is oviparous and not ovoviviparous. In both
species, the earliest stages of cleavage occur while the egg is still in the oviduct.
EMBRYONIC DEVELOPMENT OF HETERODONTUS JAPONICUS
As the title of this article indicates, we are here concerned primarily with the em-
bryology of the Japanese Bullhead Shark, as set forth in Dean’s notes and drawings; but
the observations of other authors, working mainly with H. phillipi or with H. japonicus,
will be noted for comparison. It will be evident that descriptions of the development of
H. phillipi are confined to the early stages; while practically all that is known concerning
the embryology of Heterodontus japonicus has been either discovered by Dean or made
possible by his labors.
RATE OF EMBRYONIC DEVELOPMENT
Under “Breeding Seasons”, I have already recorded observations to the effect that
eggs of H. phillipi in blastula and gastrula stages are abundant in August and September
(spring months in the southern hemisphere) and that hatching has been observed in
May. In the absence of more adequate data, this indicates a probable duration of nine
months for embryonic development. Whitley (1940) states that the period of incubation
for H. galeatus is ‘‘at least five months”.
718 Bashford Dean Memorial Volume
Barnhart (1932) notes that it takes eight to ten weeks for the young of H. francisci
to hatch from the egg case, at which time the yolk is completely absorbed and the young
shark is 14.5 inches long. Eggs have been hatched in the aquarium of the Scripps Insti-
tution at La Jolla, California, in June, September and December. Nothing is said about
the temperature of the aquarium water in comparison with that of the ocean water at the
depths where eggs are found.
In his brief manuscript containing a summary of his observations on the embryology
of Heterodontus japonicus, Dean states that the term of development (before hatching) is
reckoned at about one year, with the possibility that it may extend over a period of two
years, at an average water temperature of about 65° F. He writes that, in his estimate of
the rate of development, he was aided by the fact that eggs found in any one season are
usually in about the same stage. This latter statement may need further qualification.
Some generalities bearing on this subject are recorded under “Breeding Season” on page
712 of the present article. It is there stated that in the vicinity of Misaki spawning
occurs throughout the year, though the special spawning season is evidently the month of
March. From the original data contained in Dean’s notebook, it appears more likely that
spawning reaches its height during the month of April and continues at a rapidly reduced
rate during the months of May and June, after which it is almost negligible. As might be
expected, there is an increasing range of variation in the stages collected during each
month after the first month of spring. Hatching has been observed in April, at which
time the young shark is presumably at least a year old.
In Dean’s manuscript there is an outline for a time scale in which it was intended to
give the stage of development that predominates in each month, by reference to Balfour’s
stages in Pristiurus and other sharks. Unfortunately, the spaces left for the letters indi-
cating the stages have not been filled in. There is also a series of diagrams or outline
drawings representing developmental stages from the time of spawning to the time of
hatching. All excepting the last two (which are outlines copied from Figures 82 and 84,
plate VII) are reproduced as my Text-figures 43 to 45. Two of the original drawings are
annotated with the names of months. Fortunately these are drawings representing
stages for which data would otherwise be lacking. In the legends for Text-figures 43 to
45, I have specified the month or months in which each stage seems to predominate
according to the information at hand, but we can be fairly certain only for the months
of April, May and June.
Dean records that a total of approximately 200 embryos of Heterodontus japonicus
were collected for him at Misaki. In his notebook there is a table giving individual
records for 135 living embryos collected during April, May, June and July (up to July
6 only). This table is dated at the top, in Dean’s handwriting, “Dec. 15, 1904”. It is
probable that it does not contain any entries subsequent to this date, for all the entries
are in chronological order and there are no gaps in the series affording space for further
entries. We know that Dean was in Japan (though not continuously at Misaki) from
July to October in the year 1900; March to July in 1901; and June to October in 1905.
The Embryology of Heterodontus japonicus 719
During the season of 1900, the work was of a preliminary nature; considerable time was
spent in exploring the sea bottom in search of favorable localities for collecting. Since the
table in Dean’s notebook contains no entries later than July 6, none of the entries could
apply to specimens taken during the summer of 1900. Therefore it seems likely that all
the entries in the table apply to one season only; the spring and summer of 1901. How-
ever this may be, we have no individual records for embryos collected earlier than April
nor later than July 6 in any year, despite Dean’s statement that collecting was carried out
for him “at various intervals throughout the year”. It is known to Dean’s colleagues that
collecting for him was carried on at various times during his absences from Japan. That
some records are missing is obvious. I have found no records for individual embryos
aside from those in Dean’s table. The missing records include all stages over 35 mm. total
length, excepting a few newly hatched.
Text-figure 43.
Diagrams representing stages in the early development of Heterodontus japonicus. A, blastula stage shortly
after deposition of the egg, which occurs chiefly in March and April. The egg is drawn as seen from above,
with the upper pole, which Dean calls the animal pole, in the center. The germinal disc appears near
the equator in the upper part of the figure. Band C, stages in gastrulation and early embryo-formation
found most frequently in May.
From drawings left by Bashford Dean
Of the 135 embryos listed by Dean, 14 were taken in April, 59 in May, 20 in June,
and 42 in July (first week only). This distribution does not quite accord with Dean’s
statement, recorded in his manuscript, that ““The divers brought in the maximum number
of eggs during April and May”, unless some records for April are missing. From the
original records it appears that most of the 14 eggs collected during April were in late
cleavage, or blastula, stages (Text-figure 43a). This, according to Dean, implies that
the eggs were newly spawned. A very few had reached an early gastrula stage, and
(significantly) one was in the hatching stage. During May, a great majority of the
59 eggs collected were in gastrula stages (Text-figures 438 and 43c), but there was
a sprinkling of eggs in both younger and older stages. A few yolk sacs bore embryos old
enough to perform wriggling movements. In June, with only 20 embryos, the range of
720 Bashford Dean Memorial Volume
Text-figure 44.
Outlines representing stages in the early development of Heterodontus japonicus. The stages shown in A and
B are most abundant in collections made in June; the stage shown in C is probably representative of the
month of July. In A, the extent of the area vasculosa is indicated by dotted lines; in B and C, the principal
blood vessels are represented by solid lines.
From drawings left by Bashford Dean.
variation was greater: there were embryos of all stages from late cleavage to one of 31 mm.
total length. The average condition was somewhere between the stages shown in Text-
figures 444 and 44n. It should be noted that by this time the average condition no longer
represents accurately the rate of development of eggs spawned in April, on account of the
lag occasioned by continued spawning. Of the 42 eggs taken in July, the majority were
collected on July 3 and opened the same day; the others were taken on July 4 and opened
on July 6. Here, there are surprising numbers of gastrulae and of slightly later stages,
which can hardly be considered as representative of this month; but there are twelve
embryos ranging from 15 to 35 mm. long. For July as a whole we have no adequate data
indicating the average stage of development, but in view of what follows we assign
Text-figure 44c to this month. The original drawing reproduced as Text-figure 45 bears
the annotation ““Aug‘Sept’. The next later stage, represented by Text-figure 453, we
assign to October because the following one, portrayed in Figure 82, plate VII, is marked,
on the original, ““Nov-Dec”’.
The newly hatched young, in dorsal view, is represented by Figure 83, plate VII.
A slightly older specimen, in lateral view, is portrayed in Figure 84, plate VII. In his
manuscript Dean states: “In capsules that have long been incubated, I have found in
April the only stages where the young is about to escape from the capsule”. He records
also that “in a single instance the act of hatching was observed”. This event took place
early in April, and is described on pages 709 and 753 of the present article. It is important
to note that this specimen had been collected only a few days previously. The young
shark at hatching is said by Dean to measure about 7 inches (180 mm.) long. As indicated
by the original notes, this measurement refers to the single specimen of H. japonicus
observed in the act of hatching.
The Embryology of Heterodontus japonicus 721
Dean states that at first sight his list of embryos of various sizes seems to yield reason-
ably complete evidence that the entire term is twelve months or thereabouts. On the
other hand, he realizes that a weak spot in the evidence lies in the fact that the series of
later stages is not complete. He is not sure that stages such as those assigned to August-
September, October and November-December are the dominant ones for the months
that have been suggested. Specimens in these stages are not at all common, and the
range of size has become so varied that one cannot tell whether a stage such as the one
represented in Text-figure 45. is really the sequent of the one portrayed in Text-figure
45a, or is much older (i.e., from an egg which was deposited, say, in September of the
previous year). Development is probably much slower during the winter months. The
age of the embryo represented in Figure 82, plate VII, which is hardly less than seven or
eight months, might be 14 to 20 months. And at hatching the embryo, which can hardly
be less than 12 months old, is possibly aged 20 to 24 months.
The only direct observations on the growth rate are not in favor of the view that the
incubation period greatly exceeds one year. A late embryo in its opened capsule was
placed in an aquarium on August 10. It measured 45 mm. in total length. On October 5,
that is, within a little less than two months, it had attained a length of 110 millimeters.
This growth is so extraordinarily rapid (for a shark) that if the same rate were continued,
estimating roughly an increase in length of 30 mm. each month, the young fish would have
hatched by December or January (the young at hatching measure about 180 mm.). This
would make the entire period of incubation, assuming that the egg was spawned in April,
from nine to ten months. But the experiment was probably not conducted under strictly
natural conditions. The temperature of the aquarium must have been considerably
higher than that of the sea bottom; and if the egg, after opening of the capsule, was left
uncovered the embryo may have been better aerated than it would have been if the capsule
Text-figure 45.
Outlines representing stages in the development of Heterodontus japonicus. A, stage collected mainly during
August and September; B, stage presumably most abundant during the month of October.
From drawings left by Bashford Dean.
22 Bashford Dean Memorial Volume
had not been opened. Under these conditions development must have been almost
abnormally rapid. As a somewhat parallel case, I note that embryos and larvae of the
amphibian Cryptobranchus allegheniensis, kept during winter at moderate temperatures in
a basement, developed much more rapidly than embryos and larvae of the same species
left in their natural environment—in cavities under rocks in a stream often frozen over.
Much of the evidence here presented is complicated by the fact that egg laying may
occur at any time of the year, though most often in spring. Moreover, it is obvious that
much variation in the rate of development is to be expected because of differences in
temperature, seasonal and otherwise. We have Dean’s statement that eggs were col-
lected, in one instance, at a depth of 28 feet, and that Heterodontus japonicus is known to
inhabit depths varying from 3 to 20 fathoms (18 to 120 feet). At the maximum depth the
water is presumably much colder than it is near the surface, or in a laboratory aquarium.
Aeration of the eggs is another factor to be considered. An egg exposed to water cur-
rents, particularly an offshore current, is presumably better aerated than one shut off from
such currents. Lacking adequate data, it would be rash to attempt to estimate the
amount of variation in the rate of development due to environmental causes, but it must
be considerable.
GENERAL MODE OF DEVELOPMENT
This subtitle is inserted mainly to afford an opportunity to introduce at this point
Dean’s evaluation of his results from the study of the embryology of Heterodontus japoni-
cus, and his hopes for future accomplishments, in his own words taken from his brief and
very incomplete manuscript:
Heterodontus, although separated from its nearest genera during long ages (at least since
the earliest Mesozoic), exhibits a plan of development not differing greatly from that de-
scribed among sharks of the present time. The egg is about the same relative size, its en-
velopes are similar, its early development follows the same course, its embryos have essentially
the same forms as Scyllium, Pristiurus or Squalus. It must not, however, be concluded that
its embryology is lacking in interest, for, as will be seen in the following pages, the differences
which occur in Cestraciont development are in clear accord with its more ancient lineage, and
we will find that these differences will give us an interesting light on the puzzling question
of to what degree development may in time come to be modified. It will be seen, for example,
that a Cestraciont still retains traces of an holoblastic cleavage, and that its blastoderm still
grows around the egg before the embryo is of large size, features which stand clearly in the
gap which has separated the plan of development of recent sharks from that which occurs in
ganoids and lungfshes, a plan which, on many grounds, must also have existed in primitive
sharks. But these considerations may best be examined in later pages of our work.
In a somewhat similar vein, Haswell (1898) had previously written concerning
Heterodontus phillipi: “. . . the hope is not an unreasonably sanguine one that the em-
bryonic development of a type so ancient might exhibit some important primitive features.
With regard to the stages now described, however, any expectation of the kind cannot be
said to have been fulfilled; and what impresses one most is the extraordinary persistence
The Embryology of Heterodontus japonicus 723
of certain characters which are not known to have any vital significance.”” As an example,
he cites the “orange spot” which forms such a striking feature of the egg of an elasmo-
branch in its early stages. This, in Haswell’s opinion, has been handed down with little
change from Paleozoic times. The evidence for this view is not given, but it probably rests
on the fact that the “orange spot” appears in the eggs of genera that have been segre-
gated in different families from a very early period.
It is not from surface features alone, nor from early stages alone, that one should
look for developmental characters linking Heterodontus to the most primitive elasmo-
branchs. In studying the phylogenetic relationships of the various groups of vertebrates,
the later stages of embryonic development often yield evidence more satisfactory than
anything the early stages afford. In Heterodontus, the field of organogeny is largely
unexplored. There are, to be sure, a few contributions that deal wholly or incidentally
with the development of organ systems in Heterodontus: such as those of Osburn (1907)
on the origin of paired limbs; Luther (1909) on the musculature innervated by the trigem-
inal nerve; and de Beer (1924.1,.2 and.3) on the development of the head. Since it does
not lie within the province of the present article to review the literature on organogeny,
no attempt has been made to make this list complete.
THE EGG AND ITS MEMBRANES
The orientation of the early blastoderm of Heterodontus phillipi within the egg
capsule has been described by Haswell (1898). He states that the blastoderm, which
appears as a circular reddish-orange spot about 2 mm. in diameter, occupies a constant
position in the egg: it is always situated much nearer the broader end of the egg shell.
The extremity of the blastoderm destined to become posterior is always directed away from
the broader end of the egg shell. This indicates that the egg is anchored by the albumen
in such fashion that it is free to rotate only about an axis that corresponds to the long
axis of the capsule. In the egg of Pristiurus, the germinal disc is always situated at the
pole of the egg which is near the rounded end of the egg capsule (Leydig, 1852).
In Dean’s article entitled “Reminiscence of Holoblastic Cleavage in Heterodontus
(Cestracion) japonicus’, published in 1901, there is some ambiguity in his use of the term
‘animal pole”. This difficulty arises in part from our preconceptions, for certain features
of the egg during early development are apparently unique. In his later manuscript
Dean seldom uses the term “animal pole’’, thereby attaining greater clarity in his descrip-
tion of the egg, which follows:
The egg [of Heterodontus japonicus] measures from 40 to 50 mm. in diameter. It is pale
greenish-yellow in color, but bright red in the germinal spot [Figure 79, plate VII]. It is of
semifluid consistency, as in sharks generally, and can be removed unbroken from the capsule
only with the greatest difficulty. It is enclosed in a glistening, somewhat firm vitelline
membrane, and supported by viscid albumen, which in turn is attached to the stout capsule.
The orientation of the egg is conditioned by gravity, the germinal area [equivalent to the
“orange-yellow spot” of other Elasmobranchs] remaining near the upper pole. It probably
does not take its position [precisely] at the upper pole although this was not decided, since as
724 Bashford Dean Memorial Volume
soon as the capsule is opened, the tension maintained by the albumen is destroyed and the
germinal area probably loses its normal position. In nearly every case it remained near the
equator of the egg. The albumen is thick and glairy, transparent save at the extreme upper
and lower regions [of the capsule?]. Here it becomes opaque and is attached firmly to the
capsule. The albumen shows clearly its origin in tunics: one envelope is especially clear near
the egg, forming a whitish membrane, reminding one of the inner layer of the albumen of an
amphibian egg (e.g., Necturus). When this is ruptured the contour of the egg is disturbed.
When the albumen is in part removed, as when the upper portion of the capsule is cut away
with the attached albumen, so that the egg is better exposed, there is a relaxed pressure
which results in a flattening of the exposed surface of the egg and, in cases, gives rise to the
rupture of the vitelline membrane. In such cases the egg appears with a hernia-like expansion.
Under usual conditions an egg may be shifted about within the capsule so that the germinal
area can be seen.
As one sees from an inspection of Figures 1 to 6, plate I, there are furrows, travers-
ing the region of the upper pole, which are apparently cleavage furrows. Their pattern
suggests that this region may be a primary center of development; but it will soon be
superseded by the germinal disc, which is already undergoing segmentation and will
presently assume complete control. These subjects are fully discussed in the two
following sections.
REMINISCENCE OF TOTAL CLEAVAGE
The portion of Dean’s manuscript dealing with this topic is in a finished condition as
compared with most other parts. It is evidently a revision of his article published in
1901. In the figures illustrating that article, the outline of the germinal disc, which is
small and very faint in the original drawings, does not appear with sufficient clearness to
attract the attention of the observer, expecially since it is not labelled. In most of the
drawings, as reproduced in 1901, the outline of the germinal disc cannot be seen at all,
even with the aid of a strong reading glass. Therefore I have had some of these drawings
reproduced by lithography (Figures 1 to 6, plate I), and have inserted here the correspond-
ing portions of Dean’s manuscript without change save for the rearrangement of some
tabulated matter, the substitution of reference numerals to meet a revised arrangement
and enumeration of the figures, and the insertion of some additional references to figures.
The peculiar interest in the development of Heterodontus is that it still bears witness to
an earlier condition of holoblastic cleavage. There can be no doubt that the great size of the
egg of recent selachians is a secondary embryological character, and that the early ancestors
of sharks produced eggs which, like those of ganoids and lungfishes, were small, poor in yolk
and fertilized externally. Indeed we already know that the Palaeozoic Cladoselachians and
Acanthodians were not provided with intromittent appendages, and that therefore small
eggs and a more or less holoblastic cleavage probably then prevailed within the group of
sharks. We have found furthermore [Dean, 1906] that a recent Chimaeroid, Chimaera
colliei, undergoes in its early stages a curious process of fragmentation of the egg which can
best be explained on the ground that it represents a form of holoblastic cleavage, specialized
and retained for a new physiological function. On such evidence, accordingly, there was
The Embryology of Heterodontus japonicus
strong reason, a priori, for prophesying that in so conservative a shark as Cestracion [Hetero
dontus] there might still—in spite of the great size of the egg— persist traces of the ancestral
holoblastism. It was of peculiar interest, therefore, to find such a condition present.
The earlier stages [Figures 1 to 6, plate I; and Figure 79, plate VII] invariably showed
a series of lines (furrows) traversing the surface of the eggs in a fashion which corresponds
closely with the early superficial furrows appearing in the eggs of Amia [Dean, 1906] or, better
still, Lepidosteus [Eycleshymer, 1899]—and in these [latter?] instances there is no question
that the furrows represent cleavage.
Before, however, considering the question of the homology of these “cleavage” lines
in the egg of Cestracion [Heterodontus] we may describe their conditions in various stages.
In the ripe ovarian egg no traces of these lines occur. In an egg taken from the oviduct—the
earliest stage in my material—the furrows in the yolk region are already present, almost as
numerous as in later stages. But there is this very noteworthy difference, that in the neighbor-
hood of the (red) germinal area there appear a number of unpigmented lines and circles
[Figures 40 to 43, plate IV] occupying a wide zone between the red germinal area and the
yellow yolk region—the most conspicious of these being a white circle immediately sur-
rounding the germ [Figures 7 and 8, plate I].
As development proceeds, this entire intermediate zone becomes less and less con-
spicuous: it is later noted in the early stages of gastrulation. I believe that this zone represents
a region in which the interblastomeral spaces of the segmented germ pass over into the furrow
spaces on the surface of the yolk region. For this was clearly seen in the earliest stage which
I was able to collect (capsule taken from the oviduct); especially clear were the lines when one
carefully removes the living germ (e.g. in a spoon-shaped spatula) and examines it (in salt
solution) by transmitted light. Such a preparation will be seen in [Figure 7, plate I] from a
camera drawing. It shows a stage of late cleavage (? 7-10 cleavage) [more likely sixth to
seventh cleavage] with the blastomeres containing the red pigment situated in an irregular
central area, and with the surrounding unpigmented band traversed radially by shallow
furrows. The latter spread out peripherally and could not be traced further since the soft
yolk around the margins had escaped in the preparation. In another and older specimen,
from a capsule which was partly protruding from the oviduct, the condition of the marginal
zone could be seen more satisfactorily [Figure 8, plate I]. In this, the preparation was partly
hardened (sublimate-acetic) before it was examined by transmitted light. There could then
be seen not only the central pigmented blastomeres but in the circle surrounding them a series
of blastomeres, somewhat larger in outline and separated from one another by wider spaces.
Beyond these, and in the region of the yolk, were a number of faintly outlined biastomeres,
whose intervening spaces suddenly dilated into the beginnings of the great furrows which
traverse widely on the surface of the egg. It may be remarked that stages of or near this
period give but the faintest indication of blastomeres in the “transitional zone” if examined
as opaque objects, whether in living or in hardened material [Figure 9, plate I]; and it is clear
that the indication of these blastomeres is marked out not by actual separation of the cells, but
by shallow superficial grooves and by a thinning away of the cytoplasm in planes in which
(perhaps in earlier stages of ontogeny) cell boundaries probably existed. By this process the
yolk had become drawn into the central portion of each potential blastomere, leaving the
intervening parts transparent—conspicuous when examined by transmitted light.
Examining now a series of early stages (all drawn from living specimens) we may convince
ourselves as to the character and disposition of these larger furrows. In Figures [1 and 2,
plate I] are shown two blastulae as they appeared in the open capsule, viewed from above.
The germinal area [indicated by a tiny circle] lies nearly or quite at the margin of the
725
726
Bashford Dean Memorial Volume
drawing. I note that when the albumen is removed close to the egg (so that the surface may be
better examined) the germinal area passes out of sight below the equator of the egg. Indeed
it is quite probable that the germinal area has its normal position nearer the upper pole before
the tension of the albumen is relaxed by the rupture of the wall of the capsule. In these
stages the earliest [Figure 1, plate I] has the fewest furrows. All show the furrows clustered
in the upper part of the egg, and extending thence more or less radially toward the periphery.
In side view [Figures 3 to 5, plate I] (the egg having been rotated into this position by means
of hooked needles thrust into the albumen) the furrows are seen to pass down the sides of the
egg in nearly parallel series precisely as they do in Lepidosteus, Amia or Necturus: some of the
furrows extend lower than their fellows, and all round out, flattening at the ends. [Figure 6,
plate I, shows a somewhat oblique view of the lower hemisphere, with the furrows converging
toward the vegetal pole]. The similarity of such a stage to the blastula of a ganoid is made the
more striking by the range of color in the Cestraciont egg. The animal pole is of a pale-straw
tone, the lower hemisphere is greenish-yellow and the intermediate (equatorial) zone has usually
an orange or brownish cast. [In his notebook Dean states that the equatorial zone has a green-
ish color. For the upper hemisphere, the colors are shown in Figure 79, plate VIJ].
Another regard in which the furrows indicate their homology with cleavage lines is
their behavior with respect to the downgrowing blastoderm [a product of the germinal disc].
This begins at the side of the segmented “animal pole” of the egg, extends across it and en-
closes the egg in such a way that the [yolk] blastopore closes at nearly the opposite point on
the equator of the egg to the one where the germ was situated, in this regard suggesting the
conditions of Lepidosteus or Amia. In this connection it is to be noted that when the [yolk]
blastopore in Cestracion [Heterodontus] is closing one may see through it a few long furrows
which belong to that portion of the egg (near the equator) where the lines become nearly
parallel (Figures 52 to 56, plate V).
It is none the less an extraordinary thing to maintain that a shark’s egg, especially one as
large as [that of] Heterodontus, possesses a form of holoblastic cleavage. Accordingly it
would not be amiss to consider the objections which might be urged against such a thesis.
Let us tabulate the objections as follows, and set against them the facts favorable to the view
that a rudimentary holoblastism is present.
Concerning the Homology of the Furrows of the Egg of Heterodontus
to Cleavage Furrows of a Holoblastic Egg:
They may be surface wrinkles only.—In this event we might expect them to occur in the
mature egg, to be more or less inconstant, and to be subject to change by artificial means.
They are, however, absent in the egg about the time of fertilization. They are constant in all
eatly stages examined (about a hundred specimens). They are not altered in shape and
position by artificial means, such as pressure or tension; nor do they become obliterated
(according to observations on an opened egg which was kept alive for thirty hours). They
can be distinguished after the egg has broken, and it can then be seen that the furrows are not
superficial merely, but that they pass deep into the yolk, by actual measurement at least 1.5
mm. in the upper part of the egg. Moreover the furrows do not occur at hazard. One always
finds a central series of segments in the upper part of the egg, and in the lower part a peripheral
series, with furrows nearly parallel; occasionally, moreover, as in the egg of Lepidosteus or
Amia, several of the marginal furrows may be traced into the region of the vegetal pole and
may even traverse it [Figure 6, plate I]. These numerous, close and constant correspondences
can hardly, therefore, be without homological significance.
The Embryology of Heterodontus japonicus Teall
These furrows are known to occur in no other Selachian.—Compare, however, the segmen-
tation stages of Chimaera [Dean, 1906], and take into account the paleontological history of
Heterodont sharks. In a word it is precisely since they do occur in Heterodontus that these
furrows may well be homologous with cleavage lines.
The furrows have not been traced back into the earliest segmentation stages. —A gap in the
evidence, truly, but by no means a fatal one. In earliest stages examined a continuity has
been shown between the inter-blastomeral spaces in the germ and the circum-germinal furrows.
The furrows may have no relation to the nuclei.—We note however, that the furrows do
not occur in the egg about the time of fertilization: i.e. prior to segmentation. It has been
demonstrated that nuclei are abundant in the region beyond the germinal area, to a distance
of about 10 degrees on all sides. We have some reason to infer that they extend further peri-
pherally since the neighboring circum-germinal yolk is similar in character to that in the
region where they occur. Unhappily, however, owing to technical difficulties, the outer re-
gion of the yolk has not been sectioned. But it does not follow that, because nuclei in this
region have not been demonstrated, the furrows in question cannot be concerned with
cleavage. For such an objection would apply equally well to the case of such eggs as those of
Necturus where nuclei have not been demonstrated in the vegetal region, yet where one does
not question the homology of the furrows with cleavage lines.
The furrows may be due to the action of merocytes, which are known in Pristiurus and
Torpedo to form blastomere-like structures.—Even in this event the furrows must be classified |
broadly, I think, as within the category of cleavage lines, and hence as an expression of a holo-
blastic condition. For if an egg subdivides, when deprived of its nucleus and later provided
with a sperm nucleus, does not this division come under the general head of cleavage? There
is, however, no evidence that furrows of so distinct a type have ever been produced in
a meroblastic egg by merocytes. There is on the contrary evidence for assuming that mero-
cytic division in Cestracion [Heterodontus] would be less evident than in more modern types of
sharks. For all will agree that polyspermy, in vertebrates at least, isa secondary character and
less apt, therefore, to have been prominent in the oldest sharks, like Cestracion. Indeed, we
already know, thanks to Riickert’s studies (1899) that the migration of merocytes into the
yolk is less marked in Pristiurus (an older form) than in Torpedo (a later and derived form).
We conclude, accordingly, that the weight of the evidence is unquestionably in favor of
regarding the furrows in the early Cestraciont egg as the homologues of cleavage lines.
Among Dean’s records I find several photographs of eggs exhibiting the alleged
“holoblastic” cleavage furrows. These photographs are in part identical with those
published in Dean’s article (1901) on cleavage. Some of the photographs show the
furrows quite as clearly as they are portrayed in Dean’s drawings. But it is not likely
that these drawings were made from photographs. Inserted in Dean’s notebook there are
many carefully executed drawings of these “cleavage” stages, annotated in Dean’s
handwriting. Some correspond to the drawings already published; but few, if any,
correspond to the photographs.
In some of the drawings found in Dean’s notebook the region of the upper pole of
the egg, which Dean sometimes calls the animal pole, has the appearance of a well-defined
large blastoderm or region of micromeres, from which nearly parallel furrows radiate like
meridians down over the equatorial region (as in Figures 1 to 6, plate I). Thus the egg has
728 Bashford Dean Memorial Volume
the appearance of an egg of Lepidosteus (Eycleshymer, 1899), or of the amphibian Crypto-
branchus (Smith, 1912), in an advanced stage of cleavage. In nearly every drawing of the
egg of Heterodontus japonicus in the stages under consideration there is indicated, in
addition to the “cleavage” pattern just described, a very small circular germinal disc
similar to that of other Elasmobranchs. The germinal disc is usually situated a few
degrees above the equator. From Dean’s note and manuscript it appears that this con-
ventional germinal disc (described as reddish in H. japonicus, reddish-yellow, orange-
yellow or simply orange in other Elasmobranchs) is already cut up into blastomeres
(Figures 7 and 8, plate I). Ina preliminary sketch, found in Dean’s notebook, of the egg
represented in Figure 5, plate I, the small circular area is labelled “b’d’m” (blastoderm).
The most puzzling thing about the cleavage of the egg of Heterodontus as described
by Dean is that there are apparently two distinct centers of blastomere formation. If
there are really two, the relationship between them is not clear. On this topic Dean
(1901.1, p. 4) comments as follows: ‘There is evidence that the present position of the
germ disc is a secondary one, for in eggs just deposited, (1) it is nearer the animal pole
than in later stages; (2) there is a kind of track, whitish in color, extending from the
direction of the upper pole of the egg, suggesting therefore that the disc has shifted its
position, leaving a wake behind”. Dean (1901.1, p. 7) writes further: “Cestracion
(Heterodontus) also indicates that the change in the position of the germ disc occurred
before holoblastic cleavage was given up, and we have with it a suggestion that it was
from some new or modified physiological cause that a distinction came to arise between
the germ disc and the region of the upper pole.” Certain it is that the tiny germinal disc
soon takes the lead in the formation of the embryo.
DISCOIDAL CLEAVAGE AND THE BLASTULA
Figure 79, plate VI, in color, shows the general appearance of the egg at the begin-
ning of the stages about to be described. In this egg, the furrows traversing the general
surface assume a pattern that is not the most fortunate to illustrate Dean’s thesis that they
are cleavage furrows, but the drawing is the best one available to portray the colors as
described in Dean’s notes. In his notebook Dean has written, concerning this early stage,
that the uppermost portion of the egg is “light” (yellow) and the equatorial region is
“greenish” (yellow). The region below the equatorial zone is designated simply~ yolk”.
In the drawing, the germinal disc appears pink (Dean calls it “‘reddish”’), and it is surround-
ed by a white zone—repeatedly mentioned by Dean in his notes.
Attention must now be focussed on the progress of segmentation within the germi-
nal disc. The very early stages of cleavage in the germinal disc of Heterodontus japonicus
have not been described. These stages must occur while the egg is still in the oviduct,
before or during the formation of the capsule. The earliest stages obtained by Dean are
those illustrated in Figures 7 and 8, plate I. These eggs were taken from the body of the
fish; they were enclosed in capsules that were practically complete, and were soon to be
deposited. A later stage is portrayed in Figure 9, plate I. In this drawing the blasto-
The Embryology of Heterodontus japonicus 729
Text-figure 46.
Some stages of mitosis in the blastomeres of Heterodontus japonicus: A, metaphase or middle phase
of mitosis; B, anaphase; C, early telophase. In C, the chromosomes have begun their transfor-
mation within chromosomal vesicles.
From drawings left by Bashford Dean.
derm is surrounded by a very shallow circular groove. The type of cleavage is, of course,
discoidal. It is sufficient to add that the cleavage patterns of these blastoderms are
not essentially unlike those of other Elasmobranchs: e. g., Scyllivm as portrayed by
Ruckert, 1899, Figs. 10 and 11, pl. LII.
There is a noticeable gap between the figures thus far discussed and the one il-
lustrating the earliest gastrula stage. This gap is partly bridged by Dean’s drawing show-
ing the segmentation cavity of a blastoderm dissected off the yolk mass and viewed by
transmitted light. Upon focussing with the low power of the microscope through the
thin roof of the blastocoele, an optical section is obtained which shows that the cavity is
crescent-shaped (Figure 10, plate I).
There are no other figures, suitable for reproduction, showing the cellular structure
of the blastoderm in a later stage of cleavage; but the colored drawing reproduced as my
Figure 80, plate VII, shows the general appearance of what is presumably a late blastula
(compare Figure 44, plate IV). In Figure 80, plate VII, the blastoderm is probably con-
fined to the elliptical reddish area; but when the corresponding figure on plate IV is
Text-figure 47.
Late stages of mitosis in the blas-
toderm of Heterodontusjaponicus. .
In A, late telophase, the forma- =
tion of chromosomal vesicles is
nearly complete; in B, the chro-
mosomal vesicles of a single
daughter nucleus are represented.
From drawings left by Bashford Dean.
730 Bashford Dean Memorial Volume
B Cc
Text-figure 48.
Late stages in the reconstruction of a “resting” nucleus in the blastoderm of Heterodontus japonicus.
In A, the daughter nucleus is composed of chromosomal vesicles—some fused into larger vesicles.
In B, the process of fusion is almost complete, but maternal and paternal components are segregated
in two distinct groups. In C, the duplex character of the nucleus is indicated only by a notch
on one side.
From drawings left by Bashford Dean.
compared with those that immediately precede and follow it, one gets the impression that
the pale-yellow zone also is a part of the blastoderm. On this view, it becomes easier to
explain the round dark spot at the posterior (lower) end of Figure 80, plate VII: it may be
derived from the crescentic area (dark when viewed by reflected light) which is the optical
expression of the segmentation cavity. But one notes, in this figure, that the posterior
and lateral margins of the reddish area are slightly upraised, which is fairly convincing
evidence that this area alone constitutes the blastoderm. If we consider the blastoderm
to be confined to the reddish area, then the dark spot may be simply an oil globule.
Probably, the figure under consideration was drawn, under low magnification, as seen
through a thick layer of albumen.
It does not lie within the scope of this article, as indicated by its title, to consider the
internal development. Nevertheless, it seems desirable to bring together the scanty
available data concerning the early stages. The few drawings made from microscopic
sections, found among Dean’s records, seem of sufficient historical interest to justify their
inclusion here. These drawings (Text-figures 46 to 48) are concerned with mitosis
during cleavage. The originals, probably drawn by Dean himself, lack explanations or
labels save the words “‘Cestracion blastomeres” written below Text-figures 46a, 478 and
48B; also the words “Cestracion—budding of blastomeres” under Text-figure 474. These
explanations are in Dean’s handwriting. The drawings are not dated, but the paper is
yellow with age. In the light of our present knowledge, the transformation of chromosomes
within chromosomal vesicles is clearly portrayed in Text-figures 46c and 47a. Chromo-
somal vesicles of a single daughter nucleus are shown in Text-figure 478. Fusion, in
varying degrees, of chromosomal vesicles derived from the same parent is shown in Text-
The Embryology of Heterodontus japonicus P|
figure 48a and 488. In the latter figures the nucleus appears double, and in Text-figure
48c it is notched. These are indications of the duplex character of the nucleus, which
consists of both maternal and paternal components. Had the preceding stages of mitosis
been favorably oriented, doubtless the duplex organization of the nucleus would have been
revealed there also. At the time when Dean’s drawings were presumably made, obser-
vations of this kind on the segmenting eggs of vertebrates were rare. Fora fairly adequate
bibliography of the literature on the individuality of the germ nuclei and the history of the
chromosomal vesicles during cleavage, the reader is referred to the contributions of Rich-
ards (1917) and Smith (1929).
In an early section of this article, mention has been made of a few slides bearing
serial sections of embryos of Heterodontus (presumably japonicus). These include sagittal
sections of three blastoderms in early, advanced, and late blastula stages respectively. In
the sections, which were cut in parafhn, the early blastula measures about 1.1 mm. long,
the advanced blastula 1.3 mm., and the late blastula about 3 mm. In life these blastulae
must have been appreciably larger, since such material shrinks during the process of
preparing it for sectioning. In all essential respects the two earlier blastulae, as represent-
ed in sections, are like those of other Selachians: e.g., Torpedo and Pristiurus as portrayed
by Rickert (1899, Figs. 51 and 53, pl. LVI). They closely resemble the corresponding
stages of Heterodontus phillipi, discussed in the final paragraphs of this section. The late
blastula is imperfect, so that comparisons are unprofitable.
In a brief contribution, Haswell (1916) describes surface views of two very early
stages of cleavage in the germinal discs of eggs taken from oviducts of H. phillipi
(my Text-figure 49 and 49). He states that in both eggs the cleavage lines are entirely
confined to the area of the orange spot, and do not show any trace of a tendency to become
extended beyond its limits. Two other eggs, taken from “uteri” some weeks later, showed
more advanced stages of cleavage. Neither in these eggs, nor in those studied in 1898
(described in the next paragraph), did Haswell find any indications of furrows such as
those of H. japonicus interpreted by Dean as a reminiscence of holoblastic cleavage.
Haswell (1898) studied the later stages of cleavage in H. phillipi from eggs that had
been deposited in the sea. He states that during cleavage the blastoderm appears as
a circular reddish-orange spot, around which is a narrow light-yellow band. When this
orange spot has attained a diameter of about 2 mm. it assumes an oval shape, its longer
axis corresponding with the future long axis of the body. At its posterior end appears
A B
Text-figure 49.
Surface views of early cleavage in two blasto-
derms, A and B, of Heterodontus phillipi. The
eggs were taken from the oviducts.
After Haswell, 1916, Fig. 1.
732 Bashford Dean Memorial Volume
a
a crescentic dark area which has very much the appearance of a cleft passing through
the blastoderm. The study of sections reveals that this dark area is really a cavity, the
segmentation cavity, covered by a thin transparent roof. As the blastoderm extends, this
dark area becomes less strongly marked and gradually disappears. (It has previously been
noted that a similar crescentic “dark” area occurs also in H. japonicus at a corresponding
stage, as evidenced by a sketch, without explanation, found among Dean’s drawings. In
this sketch, dark and light areas are reversed, since the object was drawn, under low
magnification, by transmitted light). In the egg of H. phillipi the light-yellow border,
previously mentioned, extends more rapidly than the blastoderm, and soon forms a broad
zone around the latter. It is quite evident that Haswell does not consider the light-
yellow zone to be a part of the blastoderm; it is apparently the superficial expression
of the “parablast”’ (periblast).
The internal structure of some early stages in the development of H. phillipi is the
chief topic of Haswell’s article published in 1898. Beginning with a fairly early stage of
cleavage, the development of the germinal disc through the blastula and gastrula stages is
described and illustrated by figures drawn from sections. Two of these figures, represent-
ing early and late blastula stages, are reproduced here as my Text-figures 50 and 51. Their
resemblance to Dean’s sections of corresponding stages of H. japonicus has already been
pointed out.
GASTRULATION AND EARLY EMBRYOGENY
In Elasmobranchs the changes that occur during gastrulation and early embryo
formation are complex, and cannot be adequately described without recourse to serial
sections. My only information concerning these stages in Heterodontus japonicus is
obtained from Dean’s drawings of both opaque and cleared total embryos, and from one
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Text-figure 50.
Sagittal section of a blastoderm of Heterodontus phillipi in a stage showing the begin-
ning of the segmentation cavity (at the posterior end, to the right of and below
the segmented area in the figure).
ant, anterior; ect, ectoderm.
After Haswell, 1898, Fig. 1, pl. IV.
The Embryology of Heterodontus japonicus 733
Text-figure 51.
Sagittal section of a blastoderm of Heterodontus phillipi in a stage in which the segmentation
cavity is well established.
ant, anterior; para, parablast or periblast.
After Haswell, 1898, Fig. 4, pl. IV.
series of sagittal sections of a gastrula stage. It has therefore been necessary to interpret
Dean’s drawings in the light of what is known concerning the development of other
species of Elasmobranchs. The most helpful contributions are those of the Zieglers (1892
and 1902); Haswell (1898); Ruckert (1885 and 1899); and Scammon (1911).
Among Dean’s drawings, the one reproduced as Figure 11, plate I, represents the
earliest blastoderm that shows indications of gastrulation. This blastoderm is decidedly
elongate—a transient phase in its development. Its margins, constituting the embryonic
rim or germinal ring, are slightly upraised, particularly at the posterior (lower) end. At
this end a small and rather indistinct pit indicates the site of beginning invagination; but
the pit may be an artifact. The central portion of the blastoderm retains some of the
reddish color characteristic of the germinal disc of an earlier stage. The pale-yellowish
zone surrounding the blastoderm is broadest at its anterior (upper) end. It represents the
marginal portion of the periblast. The original figure bears the notation “5 mm.” in
Dean’s handwriting. This probably refers to the length of the blastoderm.
Figures 45 and 46, plate IV, show the rapid disappearance of color within the
blastoderm except for a narrow line along its border. They show also the change from an
elliptical outline to one that is approximately circular. Figure 12, plate I, represents a
blastoderm a little older than that shown in Figure 11, plate I. It is only moderately ellip-
tical, and the presence of an upraised portion at the posterior end constituting the so-
called embryonic shield indicates that it isa gastrula. The median groove traversing the
ectoderm of the embryonic shield is the neural groove. Figure 13, plate I, is slightly
later and corresponds to Figure 47, plate 1V, which shows the entire egg in color. Here,
and in the following stage (Figure 48, plate IV), one notes the extension of the blast-
oderm over the surface of the yolk. That this extension is relatively rapid may be de-
duced from the slight increase in the size of the embryo proper between the stages repre-
sented by Figures 46 to 48, plate IV.
Figure 14, plate I, represents the first of a series of embryos of H. japonicus detached
from the yolk mass, stained, cleared and mounted in toto. These embryos may have been
734 Bashford Dean Memorial Volume
drawn directly, under low magnification, by transmitted light; but in the table in Dean’s
notebook many embryos are listed as photographed and also drawn. Most of the draw-
ings must be interpreted as optical sections, so it is possible that they were drawn from
photomicrographs. Such drawings show only what can be seen by focussing at a single
level, and are sometimes difficult to interpret. It is unfortunate that, with very few
exceptions, the embryos from which Dean’s drawings were made cannot be found. As
an aid to the study of the drawings, I have examined, under both monocular and binocular
microscopes, a close series of Elasmobranch embryos, chiefly Squalus acanthias, stained
and mounted by me nearly thirty years ago.
Figure 14, plate I, represents a stage intermediate between Figures 12 and 13. It
lacks the high lights characteristic of a surface view. Posteriorly, it represents that
portion of the thickened margin of the blastoderm adjoining the embryonic shield. Here,
by a process of inturning accompanied by a limited amount of concrescence and a very
considerable amount of overgrowth, the thin rim of the early blastoderm has formed
a deeper layer, the entoderm, not shown in the drawing. In the angle between the super-
ficial layer (ectoderm) and the entoderm a middle layer, the mesoderm, is being proliferated.
The thickened margin of the blastoderm contains all three germ layers, hence it is some-
times called the germinal ring. At the posterior end of the figure a pair of dark zones, one
on each side of the mid-line, probably contain axial mesoderm. Anteriorly, a dark zone
having the form of an arch represents an optical section through upraised ectoderm at the
edge of the germinal shield. The neural groove is out of focus and is not shown.
Figure 15, plate I, represents a stage slightly later than Figure 13. It shows a well-
defined notochord, with its characteristic irregular transverse striations, extending along
the mid-line of the lower two-thirds of the figure. On each side of the notochord we
see the axial mesoderm, very thin and not ready to be cut into somites. Lateral to this, on
each side, a broad dark zone represents the inner limb of the neural folds. The outer limb
of the neural folds forms the margin of all the anterior two-thirds of the figure. The
beginning of the foregut may be present in this stage, but if so, it is not clearly shown.
The figure is possibly a ventral view.
Figure 16, plate I, is the earliest drawing showing mesoblastic somites. Of these,
four pairs are complete. In the head region the neural folds appear asymmetric. On the
left side, both outer and inner limbs of the neural folds are well shown, but on the right
side the inner limb is incomplete. Evidently the drawing represents an optical section, and
the apparent asymmetry of the neural folds is due toa slight rotation of the embryo on its
long axis. The continuation of this rotation will soon bring the embryo to lie on its left
side. Parenthetically, it may be remarked that the embryo of Torpedo, as figured by
Ziegler (1892 and 1902), tends to lie on its right side; but in my whole mounts of Squalus,
the embryo lies on its left side as in Heterodontus japonicus. In the stage under con-
sideration the beginning of the fore-gut, extending forward beneath the brain as a pocket-
like portion of the entoderm, is presumably present; but it occurs at a lower level than the
structures shown in the drawing.
The Embryology of Heterodontus japonicus 735
In Figure 16, plate I, there are some incomplete intersegmental grooves marking off
three or four (probably four) pairs of incomplete somites in front of those that are com-
plete. The anterior portion of the notochord is slightly obscured by the inner limb of the
left neural fold; but it appears to extend forward farther than the first intersegmental
groove, which is quite distinct. It is dificult to identify accurately all the limits of the
primary brain vesicles in this drawing; but it seems fairly obvious that the first inter-
segmental groove marks the posterior end of the midbrain. In none of the following
drawings do we find the somites extending so far forward, though the series often ends
anteriorly with one or two incomplete somites. The region of incomplete somites in
Text-figure. 52.
Diagram showing the relation between head somites and body somites in a larval Squalus
acanthias. The somites that degenerate in ontogeny are indicated by broken lines.
1d, dorsal moiety of the first myotome; 1v,ventral moiety of the first myotome; 2d, 2v, dorsal and ventral moieties
of the second myotome; 3v, ventral moiety of the third myotome; 7, seventh myotome; a., anterior cavities;
hyp.m., hypoglossal musculature; M., mouth; ot., otic capsule; sp., spiracle; thr., thyroid.
After Neal, 1918, Fig. 10.
Figure 16, plate 1, probably coincides with the four somites that, in Squalus, degenerate
during ontogeny. These have been figured by Neal (1918) in a diagram reproduced herein
as Text-figure 52. The occurrence, in sharks, of four anterior somites that subsequently
disappear is doubtless of evolutionary significance, indicating a metameric origin of the
posterior part of the cranium. These somites serve also to connect the anterior head
somites with the body somites and thereby establish their serial relationship.
Before proceeding further with the account of the external development of the
Japanese Bullhead Shark, it seems advisable to consider what is known concerning
the internal changes during gastrulation in Heterodontus.
The internal structure of some embryos of H. phillipi in early gastrula stages has been
studied in serial sections by Haswell (1898). Three of his figures are reproduced as my
Text-figures 53 to 55. Before considering these stages directly, it is necessary to describe
some preparations for gastrulation made by the advanced blastula.
736 Bashford Dean Memorial Volume
Text-figure 53.
Sagittal section of a blastoderm of Heterodontus phillipi in a stage in which gastrulation has just begun.
ant, anterior; ect, ectoderm; end’, parablast or periblast entoderm.
After Haswell, 1898, Fig. 6, pl. V.
The blastula represented in my Text-figure 51 (after Haswell) is not ready for gastru-
lation. Before gastrulation begins, the blastoderm increases somewhat in diameter, and the
segmentation cavity (or blastocoele) extends throughout almost its entire length. The
floor of this cavity consists of a layer of yolk with unusually fine granules, unsegmented
but containing nuclei. Haswell (1898) refers to this layer as the “parablast”’, but it is
evidently the “periblast” or “yolk syncytium” of other authors (e.g., Ziegler, 1902). As
shown in Haswell’s figure of a very late blastula, the roof of the blastocoele becomes very
thin except in its anterior third. At the posterior end of the segmentation cavity there is
a collection of cells of irregular shape. Most of these cells have evidently come from the
roof of the blastula; but Haswell states that some of them are evidently being formed from
the parablast of the floor of the cavity, and that this accumulation of cells constitutes the
starting point in the formation of the parablast entoderm (end’) in Text-figures 53 and 54).
In the embryo represented in Text-figure 53, the formation of parablast entoderm is
particularly active at the posterior end.
Text-figure 54.
Sagittal section of a blastoderm of Heterodontus phillipi in an early gastrula stage.
ant, anterior; ect, ectoderm; end, entoderm; end’, parablast (periblast) entoderm; ent, archenteric cavity.
After Haswell, 1898, Fig. 7, pl. V.
The Embryology of Heterodontus japonicus Wey
Text-figure 55.
Transverse section through the posterior portion
of a blastoderm of Heterodontus phillipi in a stage
somewhat later than the preceding, but before
the differentiation of the notochord.
ect, ectoderm; end, entoderm; ent, archenteric cavity.
After Haswell, 1898, Fig. 8, pl. V.
In Heterodontus phillipi, as in other Elasmobranchs, gastrulation takes place mainly
by a process of involution. According to Haswell (1898) the first phase of gastrulation
consists of an arching upward of the posterior portion of the blastoderm, so that where it
passes into the parablast it becomes, for a short distance, vertical. It soon inclines forward
(as illustrated in my Text-figure 53), forming the embryonic rim which extends along the
entire posterior margin of the blastoderm. At the same time the accumulation of cells at
the posterior end increases at the expense of the segmentation cavity. In the stage
represented by Text-figure 53 the segmentation cavity has become extremely shallow, and
its roof has acquired a compact epithelial character.
The stage represented by Text-figure 54 possesses a definite entoderm, hence it is
a well-established gastrula. To the present writer it seems that the cleft, separating the
poorly-defined layer of cells marked end’ from the irregular layer above, is mainly an
artifact. Text-figure 55 is a transverse section through the archenteric cavity of a stage
a little farther advanced than the one shown in Text-figure 54. It shows no new features,
but is helpful in affording a different point of view. At first the floor of the archenteric
cavity consists only of yolk; but soon the anterior portion of the archenteron will form an
entodermal pocket, the fore-gut.
Text-figure 56.
Sagittal section, approximately median, of Heterodontus (presumably japonicus) in an advanced gastrula stage.
ant, anterior; ect, ectoderm; end, endoderm; per, periblast; per’, periblast endoderm; vac, vacuole.
Drawn from a slide simply labelled Cestracion, in the collection left by Bashford Dean.
738 Bashford Dean Memorial Volume
The gastrula of Heterodontus (presumably japonicus), represented by serial sagittal
sections found among Dean’s embryological preparations, is in a stage considerably later
than Haswell’s embryo shown in median sagittal section in my Text-figure 54. A median
sagittal section of Dean’s gastrula is represented in Text-figure 56. The section cuts
through the entire length of the blastoderm, which measures 8 mm. (on the slide); but the
embryo proper, shown in the figure, is only about one millimeter long. Both ectoderm and
the definitive entoderm, as shown in the drawing, are decidedly thick; but at the anterior
end of the embryo the ectoderm gradually decreases in thickness until in the extra-
embryonic portion of the blastoderm it is a simple squamous epithelium. The periblast
is represented by a pale zone of predominantly fine yolk granules interspersed with
cytoplasm, underlying the archenteric cavity and extending a short distance anterior to it.
Beneath the archenteric cavity it is much thicker (deeper) than it is anteriorly. This
thick portion lacks nuclei, but contains a number of fairly large vacuoles. Underlying the
anterior end of the definitive entoderm, and extending forward beneath the ectoderm,
isa thin layer of irregularly shaped cells that constitute the periblast entoderm. They
seem to grade into the definitive entoderm, and perhaps contribute to it; anteriorly, the
layer becomes even thinner and in the extra-embryonic portion of the blastoderm it
is represented (in sections) by a single row of sparsely distributed cells lying between the
ectoderm and the yolk mass. Underlying the thick portion of the periblast entoderm,
a little distance anterior to the archenteric cavity, there are a few periblast cells (not
merely nuclei) imbedded in the yolk.
The advanced gastrula of Torpedo figured in median sagittal section by Ziegler (1892)
is in about the same stage as the embryo of Heterodontus japonicus represented in my
Textfigure 56. Ziegler’s figure shows the section continuing throughout the entire
length of the blastoderm. A striking difference is the much greater thickness (2 to 5
cells deep) and compactness of the periblast entoderm in the extra-embryonic portion of
the blastoderm, as compared with Dean’s gastrula in which this layer is only one cell
thick and the cells are separated by fairly wide intercellular spaces.
THE YOLK BLASTOPORE
Before going further with a description of strictly embryonic development it seems
advisable to give brief attention to the formation and closure of the yolk blastopore, which
may be regarded as a delayed phase of gastrulation.
The yolk blastopore is simply that portion of the surface of the yolk mass which,
subsequent to the beginning of gastrulation, is not yet covered by the blastoderm (Figures
46 to 59, plates IV and V). It is bounded by the rim of the blastoderm and is continuous
with the floor of the archenteric cavity. The name blastopore seems more appropriate
after the blastoderm has covered more than half the yolk mass, but the morphological re-
lations are the same in earlier stages. One reason for regarding the yolk blastopore as
related to gastrulation is that, in heavily yolk-laden eggs, circumcrescence (overgrowth of
the yolk by the blastoderm) is an important factor in gastrulation—it assists in laying
The Embryology of Heterodontus japonicus 739
down the definitive entoderm. In later stages, circumcrescence provides a protective and
vascular covering for the yolk mass. These extra-embryonic structures will be
eventually resorbed.
The yolk blastopore of Heterodontus japonicus is probably unique in that the surface
of the yolk is traversed by furrows that appear to be cleavage furrows. These are clearly
shown in Figures 46 to 56, plates [V and V. They are distinct in some of Dean’s photo-
graphs, both published and unpublished (cf. page 727). In Figures 52 to 56, plate V, the
appearance of the yolk blastopore is strikingly like that of the yolk plug of some amphibian
eggs (e.g., Cryptobranchus as described by Smith, 1912, Figs. 115 and 138 to 140). In both
cases the yolk is traversed by furrows, and the pattern is much the same. It is obvious
that in nearly all the drawings of developing eggs of H. japonicus, in stages from the
beginning of gastrulation until after the closure of the yolk blastopore (Figures 46 to 61,
plates IV and V), some of the problematical cleavage furrows are visible even after they
have been covered by the translucent blastoderm.
The closing phases of the yolk blastopore (Figures 57 to 61, plate V) are marked by
variability in its outlines and by the presence of the vitelline vessels (considered in a later
section). Figure 61, plate V, represents the final stage in the closure of the blastopore.
The site of closure is not far behind the yolk stalk. ;
In a portion of his manuscript already quoted in my section on “General Mode of
Development”, Dean states that the blastoderm of Heterodontus japonicus “still grows
around the egg before the embryo is of large size” and seems to regard this as a character of
considerable phylogenetic importance. This view implies that in more modern sharks
closure of the yolk blastopore is delayed. Some measurements of the size of the early
embryo in relation to the size of the entire blastoderm have a bearing on the problem.
The advanced gastrula of Heterodontus japonicus represented in surface view in
Figure 13, plate I, has a blastoderm about ten times as long as the embryo proper, which ts
about one millimeter long; while a gastrula of Torpedo ocellatus in about the same stage,
drawn by Ziegler (1892, Text-fig. 3) in surface view, has a blastoderm only five times its
length. A similar comparison may be made in median sagittal sections. Dean’s gastrula
represented in my Text-figure 56 has a blastoderm (extra-embryonic portion not shown in
the drawing) about eight times as long as the embryo proper; while Ziegler’s figure (1892,
Fig. 15, Taf. III) of a gastrula of Torpedo ocellatus in approximately the same stage has
a blastoderm (drawn entire) about three and one-half times the length of the embryo
proper. These measurements indicate that the blastoderm of Heterodontus japonicus
grows faster, or at least spreads out more rapidly, in proportion to the size of the embryo,
than does the blastoderm of Torpedo ocellatus.
There remains the question concerning the comparative sizes or stages of develop-
ment of embryos at the time when overgrowth of the yolk by the blastoderm is completed.
’ The egg (yolk mass) of H. japonicus in the early stages of embryonic development measures
from 40 to 50 mm. in diameter. The egg depicted in Figure 61, plate V, is in the stage in
which the yolk blastopore has just closed. As compared with the other eggs in approxt-
740 Bashford Dean Memorial Volume
mately the same stage, it has an unusually large yolk mass, probably about 50 mm. in
diameter. The length of the embryo (when straightened) equals about one-fourth of
the diameter of the yolk mass. One wishes for similar data concerning modern sharks,
but a cursory search of the literature reveals nothing that is helpful in this connection.
LATER EMBRYONIC DEVELOPMENT
The account of the embryonic development of Heterodontus japonicus has been
interrupted quite arbitrarily, following the stage with four pairs of mesoblastic somites,
in order to consider the yolk blastopore before reaching a stage too far removed from
its origin. The remaining stages of embryonic development, as represented in Dean’s
drawings, will now be considered in serial order.
Figure 17, plate I, represents a cleared embryo with 12 pairs of complete and one
pair of posterior incomplete somites. The course of the right neural fold in this figure is
not easy to follow, but it seems quite certain that the neural folds have almost met
anteriorly as well as posteriorly. What appears to bea neural fold on the right side of the
figure is the floor of the neural plate seen in optical section. According to this interpreta-
tion, the head region has rotated anticlockwise through almost 90 degrees. In the absence
of rotation, it would be impossible to obtain a side view of the beginning cephalic flexure
and the structures underlying the brain. The pocket situated ventrad and caudad
to the brain is the foregut. The arch-like anterior intestinal portal, leading from the
broad subgerminal cavity into the narrower fore-gut, is plainly visible. An embryo of
Squalus acanthias possessing the same number of somites has the neural tube almost closed
throughout its length.
Figure 18, plate I, represents a cleared embryo with 12 pairs of complete somites,
one posterior and two anterior incomplete somites. The latter appear to be undergoing
degeneration. The neural folds appear to be united in their middle thirds. Anteriorly,
the folds appear less close together than in Figure 17, and the cephalic flexure is less
pronounced; the amount of rotation in the head region is less. Evidently the brain is not
quite so far along in its development, despite the fact that some other structures are
slightly more advanced. The fore-gut and the anterior intestinal portal are well shown.
A sheet of mesoderm is found dorsal, anterior and ventral to the fore-gut; its ventral
portion is evidently mesenchymatous. The deep dent at the anterior end of the right
neural fold is an artifact.
Figure 19, plate I, represents a cleared embryo with 14 pairs of complete somites and
one pair of anterior incomplete somites. The neural tube is closed except for a short
distance at each end. There is a pronounced cephalic flexure and a beginning cervical
flexure. The fore-gut is enlarged dorso-ventrally. This drawing shows a decided under-
cutting and uplifting of both head and tail-bud.
Figure 20, plate II, represents a cleared embryo with 18 complete somites and one
anterior incomplete somite. The right side only is shown, but presumably the left side
has the same number. The cephalic and cervical flexures are slightly more pronounced
The Embryology of Heterodontus japonicus 741
than in the preceding drawing. The brain shows differentiation into the primary vesicles
(forebrain, midbrain, hindbrain) and there are indications of a secondary division of the
hindbrain into myencephalon and metencephalon. The bulge at the side of the forebrain
represents an early stage in the formation of the optic vesicle.
I have found in Dean’s collection of microscopic slides a total mount of an 18-somite
embryo labelled ‘‘Cestracion.” This appears to be the specimen from which Figure 20,
plate II, was drawn. The embryo is slightly overstained, but corresponds to the drawing
in every respect save that the small round black spot in the region of the neurenteric
canal is lacking, and the triangular dark area (mesodermal?) at the anterior end of the
fore-gut is not so sharply defined. In view of the scarcity of information concerning sizes
of the embryos represented in the plates, it is interesting to note that this 18-somite
embryo, measured on the slide, is 3.5 mm. (about one-eighth inch) long.
Figure 21, plate I, portrays in surface view an embryo of about 24 somites (one side
only). This figure, and the one immediately following, appear to be drawn at a magnifi-
cation lower than that employed for the cleared specimens that precede them. The
body of this embryo leans to the left, while the head is turned slightly to the right.
The tail bud projects for some distance beyond the posterior rim of the blastoderm, and
the head is entirely free from the underlying structures. In this embryo both cephalic
and cervical flexures have almost reached their maximum. The right optic vesicle and lens
are faintly indicated. The pronounced bulging in the hyoid region and that dorsal to
the midbrain are probably abnormal.
In Figure 22, plate II, a surface view, only 20 somites are readily visible; but in the
caudal region four or five more are faintly indicated, making a total of about 25. In
addition, there is an incomplete somite, probably degenerating, at the anterior end of the
series. This embryo appears normal save for the presence of a large bulge of the ectoderm
over the midbrain and a lesser bulge of the same kind dorsal to the anterior (incomplete)
somite. For the first time in this series, we see something like a yolk stalk—in this stage
very short and thick. The rudimentary eye is decidedly larger than in the preceding
drawing, and there is more differentiation in the branchial region. Of the visceral arches
the mandibular, hyoid and first branchial are recognizable; of the branchial grooves, the
spiracular (Y-shaped) and first branchial. The forebrain bulges a little dorsally.
Figure 23, plate II, represents a cleared embryo with at least 26 somites. It seems to
be drawn at a slightly higher magnification than the two preceding figures which are
surface views. It can scarcely be said to possess a yolk stalk since it is attached to the
yolk mass along almost the entire length of the body proper. Vitelline arteries and veins
are faintly indicated on the extra-embryonic blastoderm near the embryo. The optic
vesicle shows a distinct chorioid fissure. Dorsally, in the region of the hindbrain, there
is a somewhat indistinct otic vesicle. The blister-like elevation of the ectoderm, dorsal to
the midbrain and to the anterior part of the hindbrain, is probably abnormal. Some
neuromeres occur in the myelencephalon, immediately behind the otic vesicle. Between
the foregut and the diencephalon there is a straight bar of tissue which may represent the
742 Bashford Dean Memorial Volume
het
anlage of the epithelial hypophysis. It extends from the oral ectoderm to a slight de-
pression in the floor of the diencephalon—an evagination which may be the rudiment of
the infundibulum.
Figure 24, plate II, represents in surface view an embryo with at least 28 somites.
Unlike the preceding embryos, this one was drawn from the left side and has been re-
produced with right and left sides reversed to facilitate comparisons with other figures
on the same plate. It is evidently drawn to the same scale as Figures 21 and 22 (same
plate). There is some increase in length but little advance in external differentiation.
However, spiracular and first branchial grooves begin to look like gill-clefts. This is the
first drawing to show distinctly the region of the heart—just in front of the broad yolk
stalk. There isa slight caudal flexure. The angular projection of the forebrain is probably
abnormal.
Figure 25, plate Il, a surface view, portrays an embryo with about 35 complete
somites. Like the preceding figure, this one was drawn from the left side and has been
reproduced with right and left reversed. Here, for the first time in this series, we find
the sites of the spiracular cleft and the first and second gill-clefts sharply defined. It is
not certain that the closing plates between branchial grooves and pharyngeal pouches are
already perforated, but this seems a good place to begin referring to these fissures as
clefts instead of grooves. The cervical flexure is pretty well straightened out, but in
the cephalic flexure there is not much change. The dark spot dorsal to the first gill-cleft
(not the spiracular cleft) indicates the site of the otic vesicle. The region of the heart is
clearly indicated.
Figure 26, plate II, pictures a cleared embryo with about 37 complete somites and
one or two incomplete somites at the anterior end of the series. This drawing appears to
have been made at a higher magnification than the preceding fgure. The principal divis-
ions of the brain are fairly well shown, though not so clearly as in Figure 20 of the same
plate. One notes, in the branchial region, the entoderm-lined spiracular cleft and
gill-clefts alternating with mesodermal visceral arches. The greater size of the spiracular
cleft is noteworthy, considering its small size in the adult. In its early stages it looks like
a gillcleft, and indeed it is homologous with the gill-clefts. The notochord is clearly
visible throughout most of its length; it ends anteriorly just above the spiracular cleft.
Almost at the tip of the tail bud, the neurenteric canal is sharply outlined. Though the
hind-gut is rather vaguely defined, there is a distinct posterior intestinal portal. Auricular
and ventricular divisions of the heart can be distinguished. The optic cup shows a very
thin outer and a thick inner layer: these layers are united along the borders of the chorioid
fissure. The otic vesicle, dorsal to the first gill-slit, is quite prominent.
In front of the dorsal part of the spiracular cleft and close to the brain (Figure 26,
plate II) there is a thick-walled roughly circular sac which may be a “head cavity” or
head somite. In Elasmobranchs and perhaps in vertebrates generally, the muscles that
move the eyeball arise (Marshall, 1881; Van Wijhe, 1882; Scammon, 1911; Neal, 1918)
from mesodermal segments (head somites) which are serially homologous with the somites
The Embryology of Heterodontus japonicus 743
of the trunk (Text-figure 52, page 735). In Elasmobranchs the head somites, like the
trunk somites of vertebrates generally, are at first hollow and their cavities communicate
with the primitive coelomic cavity. In the head, this communication is by way of the
pharyngeal or visceral arches (mandibular, hyoid and branchial arches), as shown for
Torpedo in Text-figure 57a. These channels quickly close (Text-figure 57s) and the
somites become solid structures.
M. oblig. sup. M. oblig. sup.
™. rect lat.
) exe /ahy
Ovex 1
Verbindung des
Kiemenbogen-
coeloms mit dem
Cavum pericardii
Text-figure 57.
Diagrams showing the origin of eye muscles, and the extensions of the primitive coelomic
cavity into the gill-arches, in selachian embryos. In A, the cavities of the pharyngeal
arches are shown communicating with the pericardial portion of the coelomic cavity; in B,
which is a later stage, the connections of these cavities have been lost.
1, 2, 3, 4, gill-clefts; S.B.C.1—5, pharyngeal arch extensions of the coelomic cavity; ch.dors., chorda dorsalis;
oc.m., anlagen of the oculomotor muscles; M. oblig. sup. and M. rect.lat., anlagen of the superior oblique and lateral
rectus muscles respectively; ves.audit., otic vesicle.
After Corning, 1925, Figs. 222 and 223; based on Froriep’s (1902) Figs. 4 and 5 (Torpedo ocellatus).
Figure 27, plate II, portrays a cleared embryo of about 41 complete somites. Like
the preceding figure, it appears to have been drawn under unusually high magnification.
This embryo exhibits a moderate caudal and a pronounced cervical flexure—the latter
presumably unusual for this stage since it does not appear in the stages immediately
following. The optic cup shows, more distinctly than heretofore, the outer as well
as the inner layer. The otic vesicle is larger, and nearer the branchial region; it is dorsal to
the first gill-cleft. The bulbus cordis and the ventral aorta are distinctly outlined and the
latter has given rise to the first three aortic arches. The hind-gut is outlined faintly along
its ventral border and at both anterior and posterior ends of its dorsal border. The
neurenteric canal is well shown.
744 Bashford Dean Memorial Volume
Figure 28, plate II, represents a surface view of an embryo with at least 50 complete
somites. It is drawn at a magnification corresponding to Figures 24 and 25 on the same
plate. In this embryo the caudal flexure attains an unusual degree of curvature—the
posterior half of the embryo is hook-shaped. A cervical flexure is lacking, but the cephalic
flexure is slightly greater than in any previous stage. There is a yolk stalk, not shown in
the drawings that immediately precede this one, and just above the yolk stalk there ap-
pears to be a tubular midgut. Of interest are the thin roof of the medulla (not seen in
any previous stage) represented by the heavily shaded portion of the hindbrain; the
closure of the ventral portion of the spiracular cleft; and the large size of the first gill-cleft.
The second gill-cleft is of moderate size, and the sites of the future third and fourth gill-
clefts are occupied by pharyngeal grooves. If the circular pale spot on the forebrain
indicates the position of the eye, then it is nearer the dorsal end of the mandibular arch
than it has been in any preceding stage. In this surface view, one cannot be sure of the
position of the otic vesicle, but it appears to be dorsal to the first gill-cleft.
Figure 29, plate II, portrays a surface view of an embryo with about 55 complete
somites. The mid-gut is not so far advanced in its development as it is in the preceding
figure. The lower two-thirds of the spiracular cleft is closed, and there is a distinct third
gill-cleft. The mandibular arch is more prominent than it has been in previous stages.
The myelencephalon (medulla oblongata) shows prominent neuromeres. The otic vesicle
appears to be dorsal to the first branchial arch. In the last three stages studied, there has
been a steady growth of the forebrain.
Figure 30, plate II, pictures the head and anterior part of the body of a cleared embryo
drawn at a higher magnification than that employed for the surface views just considered.
The number of somites is unknown, and it is not certain that this specimen is older than
the one represented in the preceding figure. Evidently the artist had trouble in getting
a clear view of some parts of this large embryo, for the drawing does not show as much
detail as one would expect ina figure of this size. There isa slight cervical flexure and the
usual pronounced cephalic flexure. The form of the brain has undergone some changes;
in particular the telencephalon or secondary forebrain has increased in size. The spiracular
cleft is not shown. The otic vesicle is still situated dorsal to the first gill-cleft, though in
adult sharks its derivative, the membranous labyrinth, is more closely associated with
the spiracular canal; e.g., as in Chlamydoselachus (Smith, 1937, pp. 423 to 430 and
Text-figure 82.)
Figure 31, plate II, portrays a surface view of an embryo with about 74 somites—now
represented by myomeres. This embryo is the first to show a fin bud—the pectoral.
Rudiments of the first and second dorsal fins, and of a pelvic fin, are recognizable only by
comparison with the figures that follow. The tail is bordered by a continuous fin fold
out of which will emerge the anal and caudal fins. There seems to be a low fold con-
necting the rudiments of all the unpaired fins; but one cannot be sure, from the
figure, whether pectoral and pelvic fin rudiments are connected by a fin fold. The
yolk stalk is now attached to the pectoral region only, just behind the heart. The spiracu-
The Embryology of Heterodontus japonicus 745
lar cleft is closed except for a small dorsal portion. For the first time, in this series, we see
rudimentary gill- filaments projecting from gill-clefts— the first, second and third, in this
embryo. Due to differential growth of associated parts, the eye is now situated very close
to the dorsal end of the mandibular arch where a swelling indicates the anlage of the
future maxillary process. The position of the otic vesicle is no longer indicated in surface
views. There isa shallow olfactory pit. The hind-gut is fairly well defined.
Figure 32, plate I, portrays in surface view an embryo with about 85 myomeres. One
notes that the yolk stalk is more slender, and that there are five gill-clefts. Gill filaments
project from all five gill-clefts, but there are none from the spiracular cleft. The rudiment
of the maxillary process is more prominent than in the preceding stage.
Figure 33, plate II, represents a surface view of an embryo with at least 88 myomeres
(those near the tip of the tail are indistinct). This embryo shows a decided advance over
the preceding one. To be sure, no new structures have emerged save a single gill filament
protruding from the spiracular cleft; but all the embryonic structures mentioned in the
preceding drawings are present in a more advanced stage of development. The myomeres
show a higher degree of differentiation. The rudiments of the fins—pectoral, pelvic,
first and second dorsals, anal, and caudal—are recognizable at a glance, though all the
median fin rudiments appear to be connected by a fin fold. Both pectoral and pelvic fin
rudiments are very broad at the base, but they are evidently not connected by a fin fold.
One sees, more clearly than in the two preceding figures, the contour of the brain. The
yolk stalk is more slender, as one would expect in this stage. There seems to be some
injury to the cardiac region.
Figure 34, plate III, pictures in surface view an embryo somewhat older than the
one shown in the preceding figure, but evidently drawn at a lower magnification. The
myomeres are not visible. All the fin rudiments are now discrete: i.e., not connected by
a fin fold. Gill-filaments are more numerous, and some are decidedly larger. The spiracu-
lar gill-cleft reveals four or five short gill-filaments; this cleft is now somewhat farther
from the first and nearer the eye. As compared with the preceding figure, there is
a remarkable enlargement of a region of the brain comprising the mesencephalon (mid-
brain) and metencephalon (anterior division of the hindbrain, containing the cerebellum).
The olfactory pit is larger and deeper. The maxillary process of the mandibular arch is
no longer clearly defined in surface views. It extends beneath the posterior rim of the
optic cup.
An embryo in Dean’s collection, slightly older than the one represented in Figure 34,
plate III, is about 38 mm. (1.5 inches) long. Its external gill-filaments are slightly longer
than those represented in this figure.
Figure 35, plate III, shows almost maximal development of the external gill filaments.
The spiracular cleft is closer to the eye and directly posterior to it. The mouth opening,
bordered by rudimentary labial folds, is now recognizable. The pectoral fin is quite
large, and the caudal fin is very long. The dorsal fins are taller, and narrower at their
746 Bashford Dean Memorial Volume
bases, than in the preceding stages. Cartilaginous fin rays are indicated in both dorsal
fins, also in the pelvic fin.
An embryo in the same stage of development as the one represented in Figure 35,
plate III, was found in Dean’s collection. It measures about 50 mm. (2 inches) in length.
Its external gill filaments are abundant and resemble those shown in the figure.
The embryo portrayed in Figure 36, plate III, is obviously older. This is shown by
the marked development of the cartilaginous fin rays and by the increased size of the
cranium. Due to the persistence of the cephalic flexure, the mouth opening still faces
caudad as well as ventrad. The spiracular cleft, situated just behind the eye, is shown
more distinctly than in the preceding figure. Indistinct myomeres, extending to the
extreme tip of the tail fin, are indicated in the posterior half of the figure. This embryo is
remarkable for the entire absence of external gillfilaments—a deficiency that is more
striking when we observe that both the preceding and the following stages show a luxu-
riant development of these filaments. There is an indistinct lateral line.
Figure 81, plate VII, represents (in color) an embryo only slightly older than the
one just described. This beautiful figure is noteworthy in several respects. First, it
shows the extreme development of the external gill-filaments; second, a tuft of these
comprising about 9 or 10 filaments protrudes from the spiracular cleft; third, the figure
represents the oldest embryo in which the eye is known to possess a chorioid fissure;
fourth, it shows a rudimentary supraorbital ridge; fifth, the pelvic fin appears to possess
a rudimentary myxopterygium; and sixth, the figure shows the entire yolk sac.
Figure 37, plate III, is noteworthy for the size of the external gills, which are as
long, and almost as abundant, as those in the embryo just considered. In some features,
the embryo portrayed in this drawing is decidedly more advanced in its development.
This is particularly true of the mouth region. The cephalic flexure has unbent toa degree
that brings the mouth into nearly its adult position. This change is accompanied by
increased depth of the branchial and pectoral regions, so that the profile of the ventral
surface is straightened (cf. Figure 36, plate III). Only five gill flaments protrude from the
spiracular cleft. Structures in the branchial and pectoral regions are obscured by the
gillfilaments. There is a supraorbital ridge, best developed at its posterior end. Some
of the fins are larger than in the preceding stages. The lateral line is indistinct.
An embryo in Dean’s collection appears to be identical with the one represented in
Figure 37, plate III. It is about 70 mm. (2.75 inches) long. Another embryo, in Dean’s
collection, which appears slightly more advanced in its development, measures only
about 60 mm. (2.36 inches) in length. Its external gillfilaments have reached their
maximal development.
The embryo portrayed in Figure 38, plate III, shows important changes. The head,
including the branchial region, has increased in depth so that in side view the embryo is
shaped more like a tadpole. Through a sort of telescoping of the branchial and pectoral
regions, the three posterior gill-clefts have come to lie dorsal to the base of the pectoral fin,
as in the adult. The distance between the spiracular cleft and the first gill-cleft has
The Embryology of Heterodontus japonicus 747
greatly increased. The fins, excepting the caudal, are larger than in the preceding figure,
and all the fins show an advance in differentiation. The tips of the spines of the dorsal
fins are now exposed, and the ventral lobe of the caudal fin exhibits the notch that is
characteristic of adults of the genus Heterodontus. The lateral line, extending along the
side of the body, is fairly distinct, and portions of the sensory canal system of the head
are indicated by white lines in the drawing. The external gill-filaments are shorter, more
delicate, and perhaps less numerous, than in the preceding stage. Seven or eight filaments
project from the spiracular cleft. The demibranch on the anterior side of the first branchial
cleft shows some of the shortened gill-fllaments that persist in the adult. In this drawing,
the supraorbital fold would scarcely be noticed if one were not familiar with its form
in the adult fish.
One of Dean’s embryos is about 72 mm. (2.8 inches) long. It is slightly less advanced
in its general development than the one represented in Figure 38, plate III, but has
external gills that resemble those shown in this figure. Another embryo in Dean’s
collection, apparently identical with the one depicted in Figure 38, plate III, is about
78 mm. (3 inches) long.
Figure 39, plate III, represents an embryo definitely older than the preceding. This
is shown by the emergence of several new features. The body proper, and the bases of
certain fins, are covered with dermal denticles. The color pattern of the embryo at the
time of hatching is vaguely foreshadowed. The dorsal fins have acquired somewhat their
form in the adult, though in adults of this species the posterior margin of the second dorsal
is sometimes partly or wholly convex. The tips of the spines of the dorsal fins are barely
visible. If one looks sharply he may see, just behind the gill-clefts and continuing caudad
for some distance, a series of grooves parallel to the gill-clefts and spaced like them, but
not so distinct. These grooves are better shown in Figure 84, plate VII, considered
later. The supraorbital ridges are hardly noticeable and are perhaps not well develop-
ed in this embryo. The general form of the body, now approximately the same as in the
adult, differs little from that represented in the preceding figure. The spiracular
opening is not shown.
An embryo in Dean’s collection, apparently identical with the one represented in
Figure 39, plate III, is broken in two in the middle and is somewhat mutilated in this
region. It cannot be accurately measured but is about 90 mm. (3.5 inches) long.
The embryo depicted (in color) in Figure 82, plate VII, is a little older than the one
represented in Figure 39, plate III. The presence of a sizable yolk sac shows that it was
taken long before hatching. In some respects, this embryo is unique and is probably
either distorted, abnormal or inaccurately drawn. In particular, the nasal opening ap-
pears high up on the front of the head and not connected with the mouth by a nasolabial
groove. Upon comparing this figure with later stages (Figures 83 and 84, plate VII), the
size of the dermal denticles arranged in a V-shaped pattern posterior to the eye appears
exaggerated. The dorsal portion of the pelvic fin forms a finger-shaped projection pointing
dorsad. This may possibly be an upturned rudimentary myxopterygium. Aside from
748 Bashford Dean Memorial Volume
these problematical features, the figure shows a moderate advance in pigmentation and
a slight increase in the size of the pectoral and first dorsal fins. It is of interest principally
because it is the most advanced embryo figured with a yolk sac.
The stage at hatching, portrayed in Figure 83, plate VII, is discussed in a later section
of this article. The embryo represented in Figure 84, same plate, is two weeks older and
therefore the consideration of this figure is likewise deferred.
THE VITELLINE CIRCULATION
Since the vitelline circulation in Heterodontus japonicus is essentially like that of
other sharks, the diagrammatic figures by Balfour (1885) representing stages in the de-
Text-figure 58.
Diagrammatic figures showing the development of the vitelline circulation on the egg of
Pristiurus: A, early; B, intermediate; and C, advanced stages.
a, vitelline artery; v, vitelline vein; yk, yolk blastopore. The letter y (in C) marks the spot where the venous
ring and the yolk blastopore were closed bythe growth of the blastoderm.
After Balfour, 1885, Figs. 1, 2, and 3, pl. 9.
velopment of the vitelline vessels of Pristiurus will serve as an introduction to the study
of Dean’s drawings. Three of Balfour’s figures are reproduced as my Text-figure 58.
A single unpaired vitelline artery emerges from the yolk stalk and proceeds cephalad
along the blastoderm under cover of the head of the embryo (Text-figure 58a). This
arterial trunk divides to form two arcuate branches that turn toward the posterior margin
of the blastoderm. In the stage represented in Text-figure 58, the blastoderm has over-
grown the entire surface of the yolk mass excepting a small nearly circular area (yk, the
yolk blastopore) posterior to the yolk stalk. The two main arterial branches have almost
surrounded the yolk blastopore, but are situated at some distance from it. Numerous
small secondary branches grow toward the yolk blastopore, and some of these connect
The Embryology of Heterodontus japonicus 749
with small veins emptying into a venous ring close to the margin of the blastoderm.
The main trunk of the vitelline vein drains the venous ring and courses straight to the
yolk stalk.
In the stage shown in Text-figure 58c, the yolk blastopore has been entirely over-
grown by the blastoderm. The venous ring has disappeared, and the area formerly
occupied by the yolk blastopore is now traversed by a continuation of the main trunk of
the vitelline vein. This trunk now receives numerous small veins, usually joining it at
right angles. The arterial ring, formed by the two main branches of the vitelline artery,
gives off numerous secondary branches which subdivide repeatedly as they grow toward
the venules. The arterioles interdigitate with the venules or connect with them presum-
ably by means of capillaries. There are no branches extending in a centrifugal direction
from the arterial ring. The main arterial trunk does not give off side branches. The later
stages in the development of the vitelline vessels of Pristiurus need not be considered.
Dean’s series of figures depicting stages in the development of the vitelline vessels of
Heterodontus japonicus is the most extensive and detailed portrayal of these vessels in any
Elasmobranch known to the writer. Even the smallest vessels appear to be drawn with
great fidelity and accuracy, but owing to their profusion many of them, even in the cajginal
drawings, can be distinguished only by using a reading glass.
In Dean’s series of drawings, the first to show vitelline vessels is Figure 56, plate V.
In this figure two delicate arteries on each side, branches of a median unpaired vitelline
artery, proceed laterad and then caudad. These arteries give off a few short secondary
branches barely distinguishable in the drawing. The posterior artery on the right is in
process of disappearance, having lost its connection with the main trunk. The thick red
ring surrounding the yolk blastopore in this and in earlier stages is not a blood vessel; it
is the remains of the pigment of the “orange spot’’, now confined to the extreme margins
of the blastoderm.
In Figure 57, plate V, there are two branches of the vitelline arterial trunk on the
left, but only one on the right; there are only faint indications of secondary branches.
A great many very small venules (best seen with a reading glass) drain into the red zone
surrounding the yolk blastopore. Presumably the red zone now contains a venous ring
or at least a venous network.
The simple pattern of the arteries pictured in Text-figure 58a is attained, in Het-
erodontus japonicus, only after the early developmental irregularities have been smooth-
ed out. In Figure 58, plate V, we see such an arterial pattern, but the veins have attained
the stage shown in Text-figure 588. In H. japonicus the venules that drain into the venous
ring are very numerous, but they are so slender and set so closely together that individual
venules can be made out only with the aid of a reading glass. In the stage represented in
Figure 58, plate V, there is an irregular venous ring. This figure, and some of those that
follow, are complicated by the presence of the problematical “holoblastic cleavage”
pattern, described by Dean and illustrated by Figures 1 to 6, plate I, of this article. These
“cleavage” furrows have been overgrown by the blastoderm, but in the living egg they
750 Bashford Dean Memorial Volume
show through it. In the original, a spot in front of the embryo probably represents the
optical effect of an oil globule in the yolk mass. It has been removed.
In Figure 59, plate V, the pattern of both arteries and veins is essentially the same as
in the preceding figure, but the yolk blastopore is smaller and some of the venules seem to
drain into an incomplete inner venous circle. This, perhaps, is an individual variation.
The venules are longer than those delineated in the preceding figure. The vitelline vein,
crossed by the tail of the embryo, may be seen leading forward to the yolk stalk which is
attached to the pectoral region of the embryo.
Figure 60, plate V, shows right and left branches of the vitelline artery diverging
more widely than in the preceding stages; their extremities extend to the margin of the
figure. The yolk blastopore is reduced to a tiny circular area just behind the pelvic region
of the curved embryo. A venous circle is lacking, and the venules converge toward
irregular masses, colored red, closely surrounding the yolk blastopore. These masses
may, in part, represent pigment, but it seems likely that they consist mainly of extrav-
asated blood. Some of the venules begin at the extreme lower edge of the figure. The
embryo lies partly on its right side, so that a blood vessel, presumably the vitelline vein,
appears to the left of its ventral surface.
In Figure 61, plate V, the trunk and the two main branches of the vitelline artery
are more prominent than in any of the preceding figures; but the branches extend to the
opposite side of the egg, which is not represented by a drawing. The yolk blastopore has
completely disappeared. The vitelline vein receives two parallel main branches close to
the yolk stalk. The veins and venules have assumed a dendritic pattern. The round spot
underneath the middle of the embryo is probably the optical effect of an oil globule in the
yolk mass.
The egg represented in Figure 62, plate V, is anomalous. It bears two embryos
(twins) each with its own vitelline artery and vein; but the two veins drain the same
nexus, into which all the venules empty. The unpaired vitelline arterial trunk leading
toward the top of the figure is longer than any shown in earlier stages. This artery ends
in the usual two branches, but the other artery passes to the margin of the figure and
cannot be traced further.
In Figure 63, plate V, the vitelline artery passes to the opposite side of the egg
before branching. This figure, taken in connection with those that follow, indicates that
the arterial circle forms entirely on the hemisphere of the egg farther away from the yolk
stalk. The vitelline vein is still short and its manner of branching dendritic.
Figure 64, plate VI, represents a stage slightly later than the preceding, though the
vitelline artery divides before reaching the upper part of the figure. Leading to the yolk
stalk, there are two main vitelline veins; the more anterior branches of these veins are the
strongest. This is an example of a tendency, by no means universal, for the vitelline
veins to occur in two groups, right and left respectively. Figure 65, plate VI, is perhaps
intended to represent the reverse side of the same egg, since the drawings of this plate
retain their original paired arrangement; but a careful study shows that the two figures
The Embryology of Heterodontus japonicus Tal
are not entirely compatible, though they represent different aspects of two eggs in nearly
the same stage. This is the first drawing to show the arterial circle, though it may occur
in an earlier stage. The arterial circle gives off many branches that reach the margin of the
figure, but none of these appear in Figure 64, plate VI, except possibly a few connecting
with the vitelline vein. Figure 65 shows the vitelline artery giving off two side branches,
but these are not present in Figure 64. Likewise the venules of the two figures do not
correspond. The embryo, as shown by its orientation, is now free to rotate at least 90
degrees on the axis of the yolk stalk.
Figure 66 and 67, plate VI, are companion drawings. The arterial ring shown in
Figure 67 is very narrow, and its branches are numerous. Some of the arterioles reach the
surface shown in Figure 66; and conversely, some of the venules shown in profusion on
this surface interdigitate and probably connect with the arterioles on the opposite side of
the egg. There are two vitelline veins, coursing nearly parallel to each other, each with
its own system of branches.
An extreme example of the tendency for the vitelline veins to occur in two groups,
right and left, is found in the egg represented in Figure 78, plate VII. The arrangement
here reminds one of the condition found in the corresponding stage of Chlamydoselachus
(Gudger, 1940, pages 603 and 619; Figure 7, plate I; and Text-figure 4). All the smaller
vitelline veins, in Chlamydoselachus, drain into a single median vein; but two groups of
veins, right and left, are prominent.
Figures 68 and 69, plate VI, are companion figures representing different aspects of
the same egg— ina stage slightly later than the preceding. There is no essential difference
in the pattern of the vitelline vessels save that the arterial circle is nearly closed by the
coalescence of segments that have become approximated. The two main branches, right
and left, of the vitelline veins unite before reaching the yolk stalk.
Figures 70 and 71 (companion figures on plate VI) are similar to the preceding with
the exception that Figure 71 shows complete absence of the arterial circle. This has been
replaced by an extension of the main trunk of the vitelline artery. The portion of the
arterial trunk derived from the arterial circle branches profusely, while the stem portion,
shown in Figure 70, lacks branches. This figure represents the latest stage in which the
patterns of both arteries and veins retain a high degree of bilateral symmetry.
Figure 72, plate VI, shows little change from the preceding stage save that the veins
and venules are more profuse. Its companion, Figure 73, plate VI, exhibits a decided lack
of symmetry in both arteries and veins. Its most striking feature is that, on one side,
a large number of venules reach almost to the main branches of the vitelline artery.
The dark area around the head of the embryo in Figure 72 is probably the optical effect of
an oil drop in the yolk mass.
Figure 74, plate VI, shows around its margin a profuse interdigitation and intercon-
nection of arteries and veins. The same situation prevails in the upper portion of Figure
75, which shows the reverse side of the same egg. Here, as in the preceding stage, the
vitelline artery has two main, though unequal, branches. The large circular dark area
752 Bashford Dean Memorial Volume
around the base of the yolk stalk in Figure 74 probably represents the optical effect of an
oil globule in the yolk mass.
The only remaining figure showing the vitelline vessels of Heterodontus japonicus is
Figure 81, plate VII. This represents a much later stage. The large vessel on the right
side of the figure is the vitelline artery; therefore the embryo must have reversed its
original orientation on the yolk sac. A profuse system of vitelline veins is distributed to
the left side of the figure (original right side of the yolk sac). Evidently there is a similar
group on the opposite side, as in Figure 78, plate VII.
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Text-figure 59.
An embryo of Heterodontus japonicus shortly before hatching, showing its coiled condition and its
orientation within the capsule.
t T. a., respiratory aperture.
From a drawing left by Bashford Dean, but evidently not his handiwork. It has been necessary to correct the positions
of the gill-clefts, eye, mouth, and nasal aperture.
HATCHING AND THE NEWLY HATCHED YOUNG
The part played by the egg capsule in the mechanics of hatching is described, for
Heterodontus japonicus, on page 709. It has already been mentioned that, in his notebook,
Dean records the length of a newly hatched Japanese Bullhead Shark as about 7 inches
(180 mm.). This was the length of the fish observed in the act of escaping from the egg
capsule. A newly hatched fish, in dorsal view, is portrayed in Figure 83, plate VII.
The Embryology of Heterodontus japonicus Woe
Since the young fish pictured in Figure 84, plate VII, is only two weeks older, it is best
considered in this section. Dean’s observations are here quoted from his typed manuscript.
A stage shortly before hatching is shown [Text-figure 59]. The young fish is coiled
compactly, the fins wrapping around the body, the head being below |i.e., toward the small
end of the capsule], the trunk bent into a loop and the tail continued so that it approaches
the larger end of the capsule. The snout lies close to the breathing apertures of the smaller
end of the capsule, and the gill-openings are not [very] distant from the right and left aper-
tures of the capsule’s larger end. These apertures at such a stage are large, the weathering of
their margins having progressed to such a degree that a considerable current of water may
be circulated through the capsule from the smaller to the larger end. The circulation is
effected by the young fish, for in the partly opened capsule one may see with what strong
muscular effort the fish is compressing and expanding its gill-pouches, drawing the water in
through its mouth at the smaller end of the capsule and ejecting it in the opposite direction.
Text-figure 60.
Outline drawing showing the attitude of a newly hatched Heterodontus japonicus, with its head upraised and
partly out of water as if seeking to escape from the aquarium in which it was confined.
From a drawing left by Bashford Dean.
In a single instance the act of hatching was observed. An egg was brought in which
was curiously light in weight, its walls papery and studded with barnacles: at first sight it
seemed empty, but an examination showed that the larger end of the capsule had not opened.
On April 4, it was placed ina laboratory aquarium: four days later, happening to take it in my
hand, I felt it suddenly vibrate, as though it enclosed a young fish which had been alarmed by
my touching it. This movement lasted a few seconds, then the fish suddenly appeared. The
hatching took place so quickly and unexpectedly that its details were not followed. The valve
opened and closed, and there was a young fish swimming about in the aquarium. It had
emerged tail foremost, that was about all that was definitely noticed.1
A student of animal behavior would have been interested in this newly hatched fish.
For it showed the most finished instincts. It swam around the aquarium actively for about
half a minute, breathing quickly and expanding its gills. It had from the beginning the move-
‘In Dean’s original notes it is stated, in his own handwriting, that the young fish had emerged head foremost. Considering that in
this stage the yolk mass had almost entirely disappeared, it appears probable that the fish would be able to reverse its orientation within
the capsule, and thus either end might escape first from the capsule—presumably from its broad end.
754 Bashford Dean. Memorial Volume
Text-figure 61.
Attitude of a newly hatched Heterodontus japonicus, with its back arched upward, exploring the corners
of the aquarium.
From a drawing left by Bashford Dean. This drawing has been slightly modified to secure correct positions for the gill-clefts
and the pectoral fin.
ments of the grown fish, it swam easily and quickly, it readily changed direction, and I soon
found that it could swim around obstacles; and, if touched, it could draw itself backward, using
its pectorals as supports. Att first it was inclined to thrust its head out of water [Text-figure
60] as if anxious to escape,'and in doing this it showed considerable flexibility in its neck, and
it would even arch the back upward: at times it would explore the corners of the aquarium
[Text-figure 61], the head and anterior part of the body flexing downward: occasionally it
would bend the head, showing again the suppleness of the neck [Text-figure 62]. A period
of rest was next observed, then a period of activity, these alternating with more or less regu-
larity. A position of rest is shown [Text-figure 63] when the young fish raises its head,
spreads out its pectorals and depresses its unpaired fins, the tail flattened against the bottom,
the tip of the dorsals falling over on the (left) side. The latter habit may be explained in one
of two ways: either as a survival of its flatten-
ing of the fins during the period of incubation,
or asa larval adaptation by which it becomes in-
conspicuous or less easily seized by a predatory
neighbor. The young fish impressed one with
the finished character of its movements: it
Text-figure 62.
Diagram showing two attitudes of the
head of a newly hatched Heterodontus
japonicus, illustrating the flexibility of the
neck.
From a drawing left by Bashford Dean. The gill-
clefts have been redrawn in a more nearly correct
position.
The Embryology of Heterodontus japonicus 755
Text-figure 63.
A position sometimes assumed by a newly hatched Heterodontus japonicus when resting on the bottom
of the aquarium.
From a drawing left by Bashford Dean. The gill-clefts have been redrawn in a more nearly correct position.
swam easily and well, it showed varied movements of its pectorals: it bit, retreated and ad-
vanced, it stood on the defensive, and it opened its mouth widely [Text-figures 648 and 64c]
as though to inspire fear. During [ordinary] breathing [Text-figures 644] it showed normally
only the most anterior teeth.
The color of the fish at hatching is dark [Figure 83, plate VII] with a series of light
bands: it is covered with a dense “bloom” of mucus. Two weeks later [Figure 84, plate
VII] it has grown 25 mm.; it has changed color, shows a kind of opisthure', holds its fins
more rigidly. The present figure indicates that down the sides of the body, in this as in
[some] earlier stages, there is a row of (16-17) deep vertical creases immediately behind the
gillslits. They suggest a continuation of the line of the gills, with which obviously they have
nothing to do. One reflects that it would be easy for an enthusiast to construct a phylogeny in
which these deep creases fused with gut pouches and became of respiratory value. The
spiracle is still of considerable size, and the dermal denticles are prominent. The latter
condition is doubtless protective, guarding against injury from rubbing, and correlated
with a long period of incubation in a capsule.
WD
Text-figure 64.
Drawings showing the mouth of a newly hatched Heterodontus japonicus in three different poses:
A, during ordinary breathing; B, moderately and C, widely open.
From drawings left by Bashford Dean.
'Opisthure: The posterior end of the caudal axis of certain fishes and embryos of fishes, which degenerates into a rudimentary
organ, or becomes absorbed in the permanent caudal fin developed in front of it (Century Dictionary).
756 Bashford Dean Memorial Volume
In his manuscript Dean states that, at the time of hatching, the yolk sac has been
completely resorbed. A small scar (about 8 x 5 mm.) shows where it last appeared. In
a footnote to this manuscript Dean quotes Goodrich’s statement (1909, p. 132) that the
yolk sac protrudes from the ventral surface of the embryo often after birth [hatching?].
Dean gravely doubts that this occurs in sharks under normal conditions. “I have witnes-
sed birth [hatching] in the cases of Cestracion (Heterodontus), Spinax, Raja, Pristiurus,
Text-figure 65.
A young female specimen, 280 mm. (11 inches) long, of Heterodontus japonicus in the collection of the Ameri-
can Museum of Natural History. Probably it was obtained at Misaki by Bashford Dean. The color pattern
has faded considerably, and is not well shown in the photograph. The mouth cavity has been opened by
a lateral incision, here shown closed by several stitches.
Photograph, American Museum of Natural History.
and in no instance was there still an external yolk sac. Viviparous sharks will, however,
under the stress of capture frequently give birth to young more or less immature”. Very
likely, in oviparous sharks, hatching may be slightly hastened by handling the egg cap-
sules. In his original notes on Heterodontus japonicus, Dean writes concerning the fish
observed in the act of hatching: “Yolk sac, so large [size indicated by a circle 3 mm. in
diameter], yellow, apparent between pectorals”. But Dean does not definitely state that
this diminutive yolk sac protruded from the body of the fish. Perhaps it had been drawn
into the body, and the yellow color was subsequently visible through the skin.
Dean’s figure of a young H. japonicus aged two weeks after hatching (Figure 84,
plate VII) should be compared with Brevoort’s figure representing another specimen in
approximately the same stage (Text-figure 22, page 690). Dean’s specimen was 205 mm.
(8.2 inches) long, while Brevoort’s measured 216 mm. (8.5 inches). Dean’s fish wasa fe-
male, Brevoort’s a male. In the drawing Brevoort’s specimen appears to be more slender,
and the fins longer. The transverse furrows of the ventrolateral body wall are not so
numerous and well-defined in Brevoort’s figure as they are in Dean’s. The color pattern
in Brevoort’s figure approaches more nearly that of the adult as portrayed in my Text-
The Embryology of Heterodontus japonicus Woy
figure 21. Some portions of the color pattern of Brevoort’s specimen appear to be unique.
It is possible that an adequate collection of this species would reveal considerable varia-
tion in the color pattern in all stages of its development.
A 280M. YOUNG HETERODONTUS JAPONICUS
This young female (Text-figure 65) belongs to the collections of the American
Museum of Natural History and was probably procured in Japanese waters by Bashford
Dean. It is one of the specimens used by Dean for the study of the developing teeth. An
incision leading from the mouth nearly to the first gill-slit was made in order to expose the
mouth cavity. This incision was closed by large stitches with fine white thread, but still
shows as an irregular line in the photograph (Text-figure 65). Two lines, both nearly
vertical but meeting at an acute angle, at the extreme anterior end of the snout, are mere
artifacts—creases in the skin—and have nothing to do with the olfactory organ. The
fifth gill-slit is smaller and less conspicuous than the others, both in the specimen itself
and in the photograph. The spiracular opening is still large enough to be sharply defined.
The parallel vertical grooves along the side of the body posterior to the gill-slits are less
numerous, less regular and less conspicuous than they are in the specimen represented in
Figure 84, plate VII, which is considerably younger. Some careful measurements of the
specimen under consideration are given in Table II.
TABLE II
SOME MEASUREMENTS IN MILLIMETERS OF A 280-mm. FEMALE
HETERODONTUS JAPONICUS
Inoeall eng. concadocnsnsopsvevooooUgONOO SOUS ONOOUoOAODODOUDKOOODOD ODDO ACOUDHOODOODAOGGODE 280
(Greatestrwidthvofhead|(athrstipill-covers) Meee eect cient ert trier tt 44
Greatest height of head (at posterior end supraorbital ridge)... 2... 2.2220 35
Greatest height of body (in a transverse plane passing through fifth gillcovers)..............- 000s see ee ee eee 42
[Laan GH ieee. Jo posoocanncopdocodda adodson boDboboccaconoDooDDonADOboRgdQUGeOaCCODNN 17
Lard aGriniangillans.. > ccoapnanodoanodopoogdacHHoboNdoocOODSgDOUON SOO DAD OOD OODOO COORD ENODUNS 8
Baselownhrstdorsaltoverlaps|basciompectoral enn ernie e eerie retire tic ieichnercereticreth Rackets tck isle rett reer -T- 8
engthiofibaseovanallin pee ee nene eer eee etter innit kere iat taper 16
Distance between base of anal fin and ventral lobe of caudal... 0.1... eee eee eee 2
Distancefromitipitoitiplokextendedipectoraltfinsmmereeeren ieee eritiielrnerekitelteicieterrer kee tenet ices 160
Vertical distance from ventral surface to tip of extended first dorsal fin. .... 0.0.2... ccc 100
Most important for the identification of the species is the fact that the color pattern
of this 280-mm. fish is fairly well preserved (though it does not show well in the photo-
graph). The color pattern agrees in most respects with the color pattern of the younger
specimens portrayed in Figures 83 and 84, plate VII. If one ignored the color pattern and
depended entirely on Garman’s key (page 663 of the present article) one would be very
likely to classify this specimen as Heterodontus phillipi instead of H. japonicus. But the
differences in the color patterns of the two species are very great, especially in young
758 Bashford Dean Memorial Volume
specimens (compare Text-figures 8 and 9, page 668, with Figures 83 and 84, plate VII).
Garman’s key, which depends mainly on the positions of certain of the fins, was perhaps
not intended to apply to such young specimens. Changes in the spacing of the fins may
be brought about by differential growth.
EXTERNAL AND INTERNAL GILL-FILAMENTS
To the list of embryos of Heterodontus japonicus, already described, that bear ex-
ternal gill-filaments, one must add those embryos represented by Figures 66, 68, 70, 72 and
74, plate VI. In the last-named figure the external gill-filaments are very profuse.
So far as one may judge from the series of embryos portrayed in Dean’s drawings,
marked individual variations in the degree of development of the external gill-flaments of
Heterodontus japonicus are rare. To be sure, the embryo pictured in Figure 36, plate III,
is entirely lacking in external filaments; whereas in another embryo of approximately the
same general stage (Figure 81, plate VII) the external filaments attain their maximum
development. But it is probable that the condition shown in Figure 36, plate III, is
exceptional. If this embryo were left out, the remaining series (including those embryos,
already noted, which are not represented by drawings) would show a fairly regular
gradation in the development and regression of the external gill-filaments.
The latest member of this series of embryos showing external gills is the one repre-
sented in Figure 38, plate III. Therefore the external gill-flaments of Heterodontus japoni-
cus are not known to persist to such an advanced stage of general development as they
do in Chlamydoselachus (Gudger, 1940, pages 629-630 and plate VI). Of Chlamydosela-
chus, a female specimen 614 mm. long and a male specimen 538 mm. longare portrayed with
short external gills. These specimens had attained the adult form, but were not full-grown
and were probably not sexually mature. The reproductive organs of a 1398-mm. female
Chlamydoselachus dissected by me (Smith, 1937, Text-figure 85) were decidedly imma-
ture, and in a female Chlamydoselachus 1550 mm. long (ibid., Text-figure 86) they were just
approaching maturity. In these specimens, as well as in the two sexually mature females
dissected by me, the gill-flaments did not show externally with the gill-flaps closed.
The question arises, what is the relation of the external gill-filaments of the embryo
to the permanent gill-filaments of the adult? Of Chlamydoselachus, Gudger (1940, p. 639)
writes: “these so-called external gills of the frilled shark are nothing but precociously
overgrown permanent gills, which later on shorten until but a bare remnant shows beyond
the gillopening.” I have been able to examine gills of Heterodontus in critical stages of
their development and to observe that the external gill-filaments are not fundamentally
different from the rudiments of the permanent filaments, but are essentially the same
structures lengthened distally. It is better to begin with the adult stage and to trace
the history of the gill-flaments backward.
Thave had no adult specimen of H. japonicus, but I have examined the gill-filaments
in an adult H. quoyi. Here, the filaments are short and deep-set, so that the gill flaps must
be pried well apart before one can observe the filaments with a lens. The fundamental
The Embryology of Heterodontus japonicus 759
plan of these gill-flaments is not unlike that described for Chlamydoselachus (Smith 1937).
Each filament of Heterodontus is a narrow band attached by one edge to the gill-septum
which it traverses in a radial direction. Thus the filaments lie approximately parallel to
one another; they are very numerous and are set close together. The extreme distal end
of each filament stands slightly away from the gill-septum; in other words, the distal ends
are free from direct attachment to the septum. Each filament bears on both surfaces
a series of close-set parallel ridges, the lamellae, which extend transversely to the long
axis of the filament. In Heterodontus the close-set lamellae project slightly beyond the
free edge of the filament, giving it a serrated appearance.
In the 280-mm. (11-inch) young female Heterodontus japonicus the gill-filaments are
much the same as in the adult specimen of H. quoyi; but the filaments are longer and their
distal extremities project farther from the gillseptum. Except for their serrated appear-
ance, these finger-shaped extremities of the gill-filaments suggest the rudimentary filaments
of the early embryo. The filaments of this specimen are easily exposed, since they cover
a considerable extent of the gillseptum. They are not, however, visible when the gill
flap is closed.
In the 78mm. (three-inch) embryo of H. japonicus already mentioned, I found the
rudiments of the internal gill-flaments (those that persist in the adult) in connection with
external filaments (shown in Figure 38, plate III). The two kinds of gill-filaments are
continuous structures. The rudimentary internal filaments are attached, throughout all
but a small distal portion, to the gillseptum and are distinguished by the presence of
rudimentary lamellae. The distal ends of these internal filaments are continuous with the
rod-like external gillflaments, which lack lamellae.
Bearing in mind this relationship between the external gill filaments of the embryo
and the internal gill-filaments of the adult, the occurrence of gill-filaments protruding from
the spiracular cleft is conclusive evidence (if such evidence were needed) that the spiracu-
lar cleft in sharks was primitively a gill-cleft functioning in the usual manner. During
early development the spiracular cleft is as large as the
gill-clefts, with which it is serially homologous; but dur-
ing later development its external orifice becomes very
small, and the spiracular canal takes on special functions
concerned with respiration. In some specimens of Heter-
odontus the spiracle is so small that it seems vestigial.
Text-figure 66
Roof of the mouth cavity of a 78mm. (3-inch) embryo of Heter-
odontus japonicus. The dental ridge, formed by the upper jaw,
is situated between the olfactory region anteriorly and the breath-
ing valve posteriorly. The small pit, shown in the center of the
figure, leads into Rathke’s pouch.
From a drawing left by Bashford Dean.
760 Bashford Dean Memorial Volume
DEVELOPMENT OF THE TEETH
Among Dean’s drawings of Heterodontus japonicus are four figures, which were
found mounted in serial order, illustrating the development of the teeth. These are
reproduced as my Text-figures 66 to 69. There are no records concerning the original
drawings, neither accompanying the drawings nor in Dean’s notebooks.
2%;
23
Wea Gu
GULLS
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Text-figure 67. Text-figure 68
Interior of the mouth and pharynx of a young (probably recently hatched) Japanese Bullhead Shark,
Heterodontus japonicus.
Text-figure 67. Roof of the oro-pharyngeal cavity, revealing the teeth of the upper jaw, the breathing
valve, and the pharyngeal denticles.
Text-figure 68. Floor of the oro-pharyngeal cavity, showing the teeth of the lower jaw, also both oral
and pharyngeal denticles.
After drawings left by Bashford Dean.
The earliest stage, represented by Text-figure 66, represents the roof of the mouth
cavity viewed from below. This drawing was made from the 78mm. embryo, in Dean’s
collection, described and figured (Figure 38, plate III) in the present article. The lower
jaw of this embryo has been cut away in order to expose the roof of the mouth. I have
compared this dissection with Dean’s drawing (Text-figure 66) and can state that the
drawing corresponds, in every detail, with the structures revealed by the dissection.
Teeth are not yet visible; but the arch-like dental ridge (formed by the lower surface of
The Embryology of Heterodontus japonicus 761
the palatoquadrate cartilages covered with mucous membrane) is readily seen between the
olfactory region anteriorly, and what appears to be a breathing valve! posteriorly. The
small pit represented in the center of the figure presumably leads into Rathke’s pouch.
Text-figure 67, like the preceding, represents an upper jaw. It is the first drawing, of
this series, portraying teeth. Presumably, this drawing was made from a recently hatched
specimen. (For similar teeth of a recently hatched H. phillipi, observe Text-figure 13,
page 672). The anterior teeth represented in Text-figure 67 are larger than the posterior
teeth (contrary to the condition in the adult) and each anterior tooth possesses five cusps.
Posteriorly, the number of cusps grades from five tonone. More distinctly than in Text-
figure 66, the breathing valve appears divided into two main portions, anterior and pos-
terior respectively. The central third of the anterior portion is subdivided into a large
number of short lobules. The filamentous portions of the breathing valve bear an irregular
fringe of lobules.
Text-figure 68 portrays what is apparently the same stage in a lower jaw. This
drawing should be compared with Text-figure 13, showing the teeth of a recently
hatched specimen of H. phillipi. There is no sharp division between anterior (cuspidate)
and posterior (grinding) teeth, and the total number of transverse rows is less than in the
adult. The anterior two-thirds of the teeth are typically five-cusped. The extreme
posterior teeth are almost or quite lacking in cusps. In the intermediate region, the num-
ber of cusps is usually four. As in the upper jaw, the extreme posterior teeth, which lack
cusps, are smaller than the largest anterior teeth. In the absence of any drawing showing
the teeth in an earlier stage, it seems probable that most of the anterior teeth possess five
cusps from the beginning—for it is known that Dean had a fairly close series of stages from
which to select specimens for drawings. In the figure under consideration there is a row
of unusually large oral denticles situated close to the inner margin of the jaw. Between
these denticles and the teeth drawn in broad view, one may see the serrated edges of an
inconspicuous inner row of teeth.
Text-figure 69 represents the roof of the mouth cavity of the 280-mm. female Hetero
dontus japonicus portrayed in Text-figure 65, page 756. Text-figure 69 depicts faithfully
not only the form but the precise number and arrangement of the teeth in this specimen.
There are three longitudinal rows, with an extra tooth at the extreme posterior end
making a transverse row of four. The anterior teeth are still typically five-cusped. Two
transverse rows of the most posterior teeth lack cusps, but each of these teeth bears
a prominent longitudinal ridge. The posterior ridged teeth are much larger (especially
longer) than the anterior teeth. The transition between anterior (cuspidate) and posterior
(grinding) teeth is more abrupt than it is in earlier stages. The middle portion of the
anterior division of the breathing valve consists of a compact group of long finger-like
lobules—which may be seen more clearly in the specimen than in the drawing.
1T have found this problematical breathing valve not only in the 78-mm. embryo of Heterodontus japonicus, but also in the 280-mm.
specimen of the same species and in a young 368-mm. H. quoyi. I have had no opportunity to observe it in the living fish, hence cannot
state positively what is its function; but its position and structure suggest strongly that it is a breathing valve.
762 Bashford Dean Memorial Volume
In the present article, the structure of the adult teeth of Heterodontus has been
described for every species except japonicus. Teeth of young specimens (after hatching)
have been described for every species except galeatus. Teeth of an embryo of Hetero-
dontus have not been described for any species.
Upon comparing the accounts, by various authors, of the teeth of the six species of
Heterodontus, it seems to the writer that the specific differences are not very great and
Text-figure 69
Roof of the mouth of a 280-mm. (11-inch) young Heterodontus japonicus, showing teeth
of the upper jaw.
From a drawing left by Bashford Dean.
The Embryology of Heterodontus japonicus 763
that most of the observed differences are correlated with age and use. The most important
points may be summarized as follows: The most anterior of the cuspidate teeth begin, as
a rule, with five cusps, but some of the more posterior cuspidate teeth begin with only
three or four cusps. The typically five-cusped condition of the anterior teeth persists
until long after hatching. Before the adult (sexually mature) stage is reached, the number
of cusps in these teeth is reduced to three, with the central cusp most prominent. Gradu-
ally the lateral cusps become inconspicuous or even absent. With age and use (the food
consisting mainly of molluscs, crustaceans, and sea urchins) the central cusp may become
worn down until the anterior teeth, collectively, appear almost pavement-like. (The
word pavement, as used here, refers to the old-fashioned much-worn stone-block pave-
ment). The posterior or grinding teeth never have prominent cusps, and some are
entirely without cusps. The few rudimentary cusps that appear in the early stages soon
give place to a longitudinal ridge, useful in grinding the food. In older specimens, this
ridge may be entirely worn away, leaving the tooth with a smooth rounded surface.
Thus the posterior teeth become more pavement-like than the anterior teeth; in the adult
they are much larger and stronger. In their prime, the anterior teeth are well-fitted for
prehension, the posterior teeth for crushing and grinding. All the descriptions and
illustrations of both young and adult teeth emphasize the differences between anterior
and posterior teeth—differences that suggested the generic name, HETERODONTUs.
Another view (see also Text-figure 1) of the Marine Zoological Station at Misaki where
Dr. Dean studied the Japanese Bullhead Shark.
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79-98, 2 pls.
McCoy, FREDERICK.
1890 Natural history of Victoria. Melbourne and London. (Heterodontus phillipi, I, pp. 53-57,
pl. 113, text-fig.).
Mixrouno-Mactay, N., AnD Macreay, WHLLIAM.
1879 Plagiostomata of the Pacific. PartsT-II]. Proc. Linn. Soc. New South Wales, 3. (Heterodontus
phillipi, galeatus, francisci and quoyi, 306-334, 5 pls.).
1884 Idem. Proc. Linn. Soc. New South Wales, 8. (Heterodontus japonicus, 426-431, pl. ).
1886 Idem. Proc. Linn. Soc. New South Wales, 10. (Heterodontus zebra, 673-678, 2 pls.).
Muzier, J., unp Henze, J.
1841 Systematische Beschreibung der Plagiostomen. Berlin. (Heterodontus japonicus, p. 76, pl. 31).
Neat, H. V.
1918 The history of the eye muscles. Journ. Morph., 30, 433-453, 20 figs.
Nicxots, J. T., anD Murpuy, R. C.
1922 Ona collection of marine fishes from Peru. Bull. Amer. Mus. Nat. Hist., 46. (Gyropleurodus
peruanus, p. 504).
Ocisy, J. Douezas.
1890 List of the Australian Palaeichthyes, with notes on the synonymy and distribution. Proc.
Linn. Soc. New South Wales, 2. ser. 4. (Heterodontidae, p. 184).
Ospurn, Raywonp C.
1907. Observations on the origin of the paired limbs of vertebrates. Amer. Journ. Anat., 7, 171-194,
5 pls.
Ospurn, R. C., anp Nicxots, J. T-
1916 Shore fishes collected by the “Albatross” expedition in Lower California with descriptions of
new species. Bull. Amer. Mus. Nat. Hist., 35. (Gyropleurodus francisci, p. 141).
Pair, ARTHUR.
1789 The voyage of Governor Phillip to Botany Bay (Australia). London. (Heterodontus phillipi,
pp. 283-284, pl. facing p. 283).
Reean, C. Tate.
1906 ~- Aclassification of the selachian fishes. Proc. Zool. Soc. London. Pt. 2, 722-758, text-figs.
1908 A synopsis of the sharkso f the family Cestraciontidae. Ann. Mag. Nat. Hist., 8. Ser. 1,
493-497.
Ricuarps, A.
1917. The history of the chromosomal vesicles in Fundulus, and the theory of the genetic continuity
of the chromosomes. Biol. Bull., 32, 249-291, 4 pls.
RUcxert, JOHANN.
1885 Zur Keimblattbildung bei Selachiern. Ein Beitrag zur Lehre vom Periblast. $.B. Ges. Morphol.
Physiol., 1, 48-104, figs.
1899 Die erste Entwickelung des Eies der Elasmobranchier. (In Festschrift zum siebenzigsten
Geburtstag Carl von Kupffer, Jena, pp. 581-704, 8 pls., 7 text-figs.).
The Embryology of Heterodontus japonicus 769
SAVILLE-KEentT, W.
1897 The naturalist in Australia. London. (Cestracion, pp. 192-194, fig.).
ScamMMon, RICHARD E.
1911 Normal plates of the development of Squalus acanthias. (In Keibel’s Normentafeln zur
Entwickelungsgeschichte der Wirbeltiere, Jena. 12. Heft, 140 pp., 4 pls., 26 text-figs.).
SreBOLpD, Poitier FRANZ.
1850 Fauna japonica: Lugduni Batavorum. Pisces (Cestracion phillipi, p. 304).
SmitH, BertTRAM G.
1912 The embryology of Cryptobranchus allegheniensis. Part II. General embryonic and larval
development, with special reference to external features. Journ. Morph., 23, 455-579, 8 pls.,
148 text-figs.
1929 The history of the chromosomal vesicles in the segmenting egg of Cryptobranchus allegheniensis.
Journ. Morphol. Physiol., 47, 89-133, 6 pls.
1937. The anatomy of the frilled shark, Chlamydoselachus anguineus Garman. Bashford Dean Me-
morial Volume: Archaic Fishes. WII, 331-520, 7 plates, 128 text-figs.
STEINDACHNER, FRANZ.
1896 Bericht ueber die wahrend der Reise Sr. Maj. Schiff “Aurora” von Dr. C. Ritter v. Mieros-
zewski in den Jahren 1895 und 1896 gesammelten Fische. Ann. K. K. Naturhist. Hofmus.
Wien, 11. (Heterodontus japonicus, p. 224). :
STRUVER, JOHANNES.
1864 Beschreibung des Heterodontus phillipi Bl. (Cestracion phillipi Bl.) mit Riicksicht auf seine
fossilen Verwandten. Nova Acta Akad. Leopold-Carol., 23, 412-416, 2 pls.
VALENCIENNES, A.
1855 Ichthyologie. (In Du Petit-Thouars, A. Voyage autour du monde sur... la Venus, pendant...
1836-39). Paris. (Cestracion pantherinus, XV, Zoologie (1855), pp. 350-351; Poissons, Atlas
(1846), fig. 10, pl. 10).
Van Wye), J. W.
1882 Ueber die Mesodermsegmente und die Entwicklung der Nerven des Selachierkopfes. Verh.
K. Akad. Wet., Amsterdam, 22, 1-50, 5 pls.
Watrte, Epcar R.
1896 On the egg cases of some Port Jackson sharks. Journ. Linn. Soc. London, 26, 325-329, pl. 12.
1898 Scientific report on the fishes. (In Report upon trawling operations off the coast of New
South Wales, . . . carried on by H.M.C.S. Thetis”). Sydney. (H. phillipi and H. galeatus, p.
53).
1899 Scientific results of the trawling expedition of H.M.C.S. “Thetis”. Fishes. Mem. Australian
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Wauittey, Grsert P.
1938 The eggs of Australian sharks and rays. Australian Mus. Mag., 6. (Heterodontus p. 373).
1940 The fishes of Australia, Part 1: The sharks, rays, devil-fish and other primitive fishes of Aus-
tralia and New Zealand. Sydney. Roy. Zool. Soc. New South Wales. 280 pp., 303 figs.
Woopwarp, A. SMITH.
1886 On the relations of the mandibular and hyoid arches in a Cretaceous shark (Hybodus dubrisien-
sis). Proc. Zool. Soc. London, 218-224, pl.
770
1889
1891
1916
1921
Bashford Dean Memorial Volume
Catalogue of the fossil fishes in the British Museum. London. Part 1, Elasmobranchii,
474 pp., 16 pls., 13 text-figs.
Hybodont and cestraciont sharks of the Cretaceous period. Proc. Yorkshire Geol. and Polytech.
Soc., 12, 62-68, 2 pls.
Fossil fishes of the English Wealden and Purbeck formation. Part 1. Monog. Paleontog. Soc.,
69. (Skull of Hybodus basanus Egerton, pp. 6 and 7, fig. 3).
Observations on some extinct elasmobranch fishes. Proc. Linn. Soc. London, 133. sess., 29-39,
4 figs.
ZIEGLER, HEINRICH ERNST.
1902
Lehrbuch der vergleichenden Entwickelungsgeschichte der niederen Wirbeltiere. Jena.
(Selachians, pp. 101-152, 55 figs.).
ZigEGuLER, H. E., uND ZIEGLER, F.
1892
Beitrage zur Entwickelungsgeschichte von Torpedo. Arch. Mikr. Anat., 39, 56-102, 2 Taf.
ZITTEL, KARL A. VON.
1911
1923
1932
Grundztige der Palaeontologie. Munchen und Berlin. II, Vertebrata—Pisces. (Hybodontidae
and Cestraciontidae, pp. 53-57, 11 text-figs.).
Idem. (Hybodontidae und Cestraciontidae, pp. 58-63, 11 text-figs.).
Text-book of palaeontology. Translated and edited by Charles R. Eastman. Second English
Edition revised, with additions, by Arthur Smith Woodward. London. II. Vertebrata-
Pisces. (Hybodontidae and Cestraciontidae, pp. 65—71, 12 text-figs.).
Rei
EMBRYOLOGY OF HETERODONTUS JAPONICUS
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
Fig.
IU
12.
13%
14.
15.
16.
17.
18.
19.
READE Ss!
EARLY DEVELOPMENT OF THE EGG OF HETERODONTUS JAPONICUS
Egg taken at time of deposition. Polar view of upper hemisphere. The germinal disc (“orange
spot’’) is indicated by a tiny circle close to top of figure.
Upper hemisphere of an egg ina slightly later stage. The germinal disc is situated on the side of the
egg away from the observer. It is indicated, as if seen through the egg, by a tiny dotted circle
near the right hand margin of the figure.
Lateral view of an egg ina stage between Figures 1 and 2. The position of the germinal disc is not
indicated.
Lateral view of an egg similar to the one shown in Figure 3. The germinal disc is indicated by
a small dark spot on the right of the figure.
An egg shown in lateral, slightly oblique, view. The germinal disc is indicated, as if seen through
the egg, by a dotted circle in the upper right quadrant of the figure.
An egg in a slightly later stage, oriented with ordinarily lower pole nearly uppermost. The
germinal disc is situated on the side of the egg away from the observer. It is indicated by a tiny
dotted circle in the upper left quadrant of the figure.
. Figs. 1 to 6 have been published by Dean in the Annotationes Zoologicae Japonensis, 1901, vol. 4. They show furrows
interpreted by Dean as a reminiscence of holoblastic cleavage. Eggs in these stages vary from 40 to 50 millimeters
in diameter.
The earliest observed stage of cleavage in the germinal disc. This region, constituting the early
blastoderm, was removed from the yolk mass. Viewed by transmitted light, it was drawn,
under magnification, in natural colors.
A later stage in the segmentation of the germinal disc. The blastoderm, removed from the egg
and viewed by transmitted light, was drawn under magnification in natural colors.
Slightly later stage of cleavage in a germinal disc viewed as an opaque object.
Blastoderm in an advanced cleavage stage, removed from the yolk and viewed by transmitted
light. The crescentic light area in lower part of figure is the blastocoele seen by focussing down-
ward through its roof.
Elongate blastoderm, perhaps ready for gastrulation, viewed as an opaque object and drawn in
natural colors. This blastoderm is 5 mm. long. The pale area surrounding it is the marginal
zone of the periblast.
Surface view of a blastoderm in an early stage of gastrulation. Note, at the posterior (lower) end,
the neural groove bordered by upraised neural folds.
Surface view of a blastoderm, with rudimentary embryo, slightly later than the preceding.
Optical section through embryonic region in a stage intermediate between Figures 12 and 13. This
figure, like the remaining ones of this plate, was drawn from a cleared preparation.
Optical section of an embryo slightly later than the one shown in Figure 13.
Optical section of an embryo with 4 pairs of complete mesoblastic somites.
Optical section of an embryo with 12 pairs of complete somites.
Optical section of an embryo with 14 or 15 pairs of somites.
Optical section of an embryo with 15 or 16 pairs of somites.
ArticLe VIII, Prarte I.
A. Hoen & Co., Lrrn.
EMBRYOLOGY OF HETERODONTUS JAPONICUS
’
BEANE I
EMBRYOLOGY OF HETERODONTUS JAPONICUS
Fig.
REAR E SI
LATER EMBRYOS OF HETERODONTUS JAPONICUS
A cleared embryo with 18 complete somites. Measured on the slide, it is 3.5 mm. (about one-eighth
inch) long.
Surface view of an embryo with about 24 somites.
Like some of the embryos represented in the surface views that follow, this one appears to have been drawn at a lower
magnification than that used for cleared preparations.
Surface view of an embryo with about 25 somites.
A cleared embryo with at least 26 somites.
Surface view of an embryo with at least 28 somites.
This figure was drawn from the left side, but it has been reversed to facilitate comparison with other figures on this plate.
Surface view of an embryo with about 35 somites. This figure, like the preceding, was drawn from
the left side but has been reversed.
A cleared embryo with about 37 complete somites.
An embryo with about 41 complete somites, drawn after being cleared.
Surface view of an embryo with at least 50 complete somites.
An embryo with about 55 complete somites, drawn in surface view.
Head and anterior part of the body of a cleared embryo. The number of somites is unknown.
Surface view of an embryo with about 74 somites, now represented by myomeres.
An embryo with about 85 myomeres, drawn in surface view.
Since all the figures of this plate are lateral views, the number of somites (in later stages represented by myomeres) is
recorded for one side only.
2 Dean Memoriat VoLUME a ArmicLe VIII, Prate II.
BasHrorp Dean, Dir. A. Hoen & Co., Litn.
EMBRYOLOGY OF HETERODONTUS JAPONICUS
>
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i Wy
Les 100
EMBRYOLOGY OF HETERODONTUS JAPONICUS
Fig.
33.
. 34.
ig. 35.
S Bish
ig. 39.
PLATE III
LATE EMBRYOS OF HETERODONTUS JAPONICUS
An embryo with at least 88 myomeres (those near the tip of the tail are indistinct).
An embryo somewhat later than the preceding. The myomeres are not visible externally.
Another embryo, in Dean’s collection, slightly older than the one portrayed here, but younger than the one represented
in the following figure, measures 38 mm. (about one and one-half inches) long.
An embryo later than the one shown in the preceding figure. Except at the tip of the tail, the
myomeres are not visible externally.
Another embryo in the same stage of development, found in Dean’s collection, measures about 50 mm. (two inches) long.
An embryo, with myomeres visible only in the posterior half of the figure. The absence of ex-
ternal gill filaments in this stage is unusual.
An embryo with profuse external gills. It measures about 70 mm. (two and three-fourths inches)
long.
This embryo is approximately 78 mm. (three inches) long. It has shorter and more delicate external
gills.
Note the lack of external gills in this embryo, which is about 90 mm. (three and one-half inches) long.
moe ey aie FS Li ae a
ArticLte VIII, Prare III.
Basurorp Dean, Dir. A. Hoen & Co., Litn.
EMBRYOLOGY OF HETERODONTUS JAPONICUS
AEE SY)
EMBRYOLOGY OF HETERODONTUS JAPONICUS
PEASE RIV,
ENTIRE EGGS OF HETERODONTUS JAPONICUS
SHOWING THE RELATIONS OF THE EMBRYO AND
THE OVERGROWTH OF THE YOLK MASS BY THE BLASTODERM
Figs. 40 to 42. Upper hemisphere of eggs taken shortly after deposition. The germinal disc or “orange spot”
is presumably undergoing cleavage. In Figures 40 and 41, the disc is surrounded by concentric
white zones; in Figure 42, by a single white zone (periblast?).
Fig. 43. A slightly older egg in which the germinal disc is in a late blastula stage.
Fig. 44. The germinal disc or blastoderm is now almost ready for gastrulation.
For larger and more accurate drawings of blastoderms in approximately the same stage, see Figure 11, plate I, and
Figure 80, plate VII.
Fig. 45. Anegg slightly later than the preceding. The blastoderm is larger, and is circular in outline.
Fig. 46. This blastoderm is much larger than the preceding one. Its posterior (lower) margin is upraised
and is in a very early stage of gastrulation. See also Figure 12, plate I.
Fig. 47. A still larger blastoderm showing at its posterior edge the upraised embryonic area. For details
see Figures 13 and 14, plate I.
Fig. 48. There is shown here a marked increase in the size of the blastoderm. The embryo shows a definite
head region. An embryo in approximately the same stage is shown in detail in Figure 16, plate I.
Figs. 49 to 51. These figures show the blastoderm spreading over a hemisphere of the egg while the embryo,
situated at the slight notch in the posterior margin of the blastoderm, is still very small and cannot
be accurately delineated on this scale. The three stages are probably equivalent to Figures 22,
24, and 25, plate II.
The drawings of this plate are in natural colors, save that the embryos represented in Figures 49 to 51, which in life are
colorless and translucent, are portrayed in opaque white. All the drawings are reproduced about natural size.
In all the figures, the yolk mass shows the furrows interpreted, by Dean, as a reminiscence of holoblastic cleavage.
DEAN Memoriat Votume ARTICLE VIII, Prare IV.
40 41 42
43 44 45
46 47 48
49 50 51
Basurorp Dean, Dir. A. Hoey & Co., Lrtn.
EMBRYOLOGY OF HETERODONTUS JAPONICUS
PLATTS, \y/
EMBRYOLOGY OF HETERODONTUS JAPONICUS
Fig.
Fig.
Fig.
Fig.
5
5 eek
. 34.
5 DBs
5 SLO:
> Sp
ig. 58.
. 59.
60.
61.
62.
63.
AL /ANIN 8) \W/
ENTIRE EGGS OF HETERODONTUS JAPONICUS
SHOWING CLOSURE OF YOLK BLASTOPORE
AND ORIGIN OF VITELLINE VESSELS
The blastoderm covers more than a hemisphere of the yolk mass. The stage of embryonic devel-
opment is perhaps equivalent to that shown in Figure 26, plate II.
In this figure the yolk blastopore is appreciably smaller, though the embryo is no larger than the
one represented in the preceding figure.
Here the embryo appears to be in a stage slightly younger than the one shown in Figure 53,
though the yolk blastopore is smaller.
In this figure the embryo is in a stage approximately the same as the preceding.
This is the first stage showing vitelline vessels, here entirely arterial. The main arterial trunk is
not visible. There are two pairs of secondary vitelline arteries, right and left. The embryo is
larger than the one shown in the preceding figure.
This figure shows a decided increase in the size of the embryo and in the degree of closure of the
blastopore. There are two vitelline arteries on the left, but only one on the right. A venous
ring, surrounding the yolk blastopore, is in process of formation.
The main trunk of the vitelline artery is shown proceeding forward from the yolk stalk, and
branching to form only one pair of arcuate arteries. A multitude of radially-directed vitelline
venules drain into the venous ring.
The yolk blastopore is nearly closed. There is no change in the arterial pattern, but the venules
are further developed. The embryo is in approximately the same stage as the one represented in
Figure 29, plate II.
The venous ring has contracted almost to the point of disappearance. The arterial pattern is
unchanged. The embryo is decidedly larger than the one shown in the preceding figure.
In this figure the vitelline vessels are especially well shown. Right and left vitelline veins extend
to the margin of the figure. There are two main branches of the vitelline vein, extending from
the plexiform group of venules to the yolk stalk.
An egg with two embryos (identical twins), perhaps with a single tail. Each embryo has its own
vitelline artery and vein, but the veins drain the same nexus of venules.
The arterial vitelline trunk passes unbranched to the other side of the egg. There is a single
vitelline vein draining a dendritic group of venules. The embryo still heads in the direction of
the vitelline artery.
Figures 52 to 59 show stages in the closure of the yolk blastopore. In Figures 52 to 56 the problematical “cleavage”
furrows of the yolk are conspicuous in the yolk blastopore. In Figures 53 and 54 some of these furrows show faintly,
and in Figures 58 and 59 many of them show conspicuously through the translucent blastoderm.
Figures 56 to 63 show early stages in the development of the vitelline vessels. In some of these drawings, the pattern
a ie vessels is more or less obscured by the presence of “cleavage” furrows in the yolk, which show through the
astoderm.
All these drawings are in natural colors save that the embryos, which in life are colorless and translucent, are portrayed
in Greque white. With the possible exception of Figures 58, 59 and 60, all the drawings are here reproduced about
natural size.
Dean Memorrat Votume
55
61
Basnrorp Dean, Dir.
53
56
59
EMBRYOLOGY OF HETERODONTUS JAPONICUS
54
60
63
ArTICLE VIII, Prate V.
A. Hoen & Co., Litn.
bellies, \V/IL
EMBRYOLOGY OF HETERODONTUS JAPONICUS
Fig. 64.
Fig. 65.
Fig. 66.
Fig. 67.
Fig. 68.
Fig. 69.
Fig. 70.
Fig. 71.
Fig. 72.
Fig. 73.
Fig. 74.
Fig. 75.
PLAIN W/L
FURTHER DEVELOPMENT OF THE VITELLINE VESSELS
IN HETERODONTUS JAPONICUS
In this figure the embryo, for the first time in this series, lies at right angles to the direction of
the vitelline artery, showing that the embryo is able to rotate by twisting the yolk stalk. The
vitelline artery branches before reaching the margin of the figure. There are two vitelline
veins leading to the yolk stalk.
An egg in nearly the same stage as the preceding, showing the hemisphere opposite the one to
which the embryo is attached. The two main branches of the vitelline artery have joined an-
teriorly to form the arterial circle.
A later stage in which the arterial pattern resembles that shown in Figure 64, while the branching
of the vitelline veins is much more profuse and extensive.
Opposite hemisphere of the egg represented in the preceding figure, showing the convergence of
right and left sides of the arterial circle, which is profusely branched.
Here the embryo has been tilted to expose the yolk stalk, which shows the main trunk of the
vitelline veins. The vitelline artery does not branch before passing to the other hemisphere of
the egg.
The opposite hemisphere of the egg portrayed in the preceding figure. The arterial circle is nearly
obliterated by the coalescence of right and left sides.
The arterial and venous vitelline trunks are here seen pursuing parallel courses as they enter the
yolk stalk. The larger branches of the vitelline vein occur in two groups, right and left.
The opposite hemisphere of the egg represented in the preceding figure. The right and left sides of
the arterial circle have coalesced to form an extension of the main arterial trunk.
Both arterial and venous patterns are similar to those shown in Figure 70, but the branching of the
veins is more profuse.
The opposite hemisphere of the egg depicted in the preceding figure, showing a symmetrical
branching of the vitelline artery.
In this figure there is a fairly long vitelline vein having side branches. The embryo is in a stage
slightly older than the one represented in Figure 35, plate III.
Opposite hemisphere of the egg portrayed in the preceding figure. The pattern of the arterial
branching is nearly symmetrical, though quite unlike that shown in Figure 71.
All the figures on this plate are in natural colors. The drawings are reproduced about natural size.
Dean Memorrat VotumE ArticLe VIII, Prate VI.
BasHForp Dean, Dir.
A. Hoen & Co., Lrru.
EMBRYOLOGY OF HETERODONTUS JAPONICUS
eat
y Iie He
LAIe, SVU
EMBRYOLOGY OF HETERODONTUS JAPONICUS
Fig. 84.
PEARESVAl
EGG CAPSULES, EGGS, EMBRYOS
AND NEWLY HATCHED YOUNG OF HETERODONTUS JAPONICUS
An egg capsule in side view. The arrow points towards the respiratory groove, just beginning to
deepen and lengthen into the respiratory cleft. The length of the capsule varies from 120 to
180 mm. (four to seven inches).
Oral, upper or proximal view (showing the larger end) of the capsule.
An egg case opened to show the yolk sac and embryo within.
Upper hemisphere of an egg at the time of deposition. This figure shows the tiny germinal disc
(reddish, surrounded by a white zone) and some problematical furrows distributed over the
greater part of the surface of the yolk.
Reproduced about four-fifths natural size.
A late blastula drawn as an opaque object seen through a layer of albumen. The blastoderm is
limited to the reddish area, which is surrounded by a pale yellowish zone, the periblast.
Advanced embryo with yolk stalk and yolk sac. The figure is slightly larger than natural size.
The external gill-flaments have reached their maximal development.
Later embryo with yolk stalk and yolk sac. In some respects (e.g., the position of the nasal apertures)
this embryo is either distorted, abnormal or incorrectly drawn.
Dorsal view of a newly hatched Heterodontus japonicus. Its length isabout 180 mm. (seven inches).
Lateral view of a young female Heterodontus japonicus, about two weeks after hatching. Its length
is about 205 mm. (eight inches).
All the figures of this plate are in natural colors.
DEAN Memoria VoLuME ArTICLE VIII, Prare VII.
Basurorp Dean, Dir. A. Hoen & Co., Lrtn.
EMBRYOLOGY OF HETERODONTUS JAPONICUS
ANALYTICAL SUBJECT INDEX
The Dean Memorial Volume is so large and heavy that it seems advisable that it be bound as Part I containing
Articles I, II, II, IV and V; and Part II containing Articles VI, VII and VIII together with the Index. The
pagination is continuous and Part II begins with page 331.
Abel, O.,
on Dinichthys, 176, 180
Heterostius, 180
Acanthaspida, 157, 169, 177, 199, 200, 208
carapace, 179, 210
fin, dorsal, 198
Acanthaspis,
fin, 198
scales, 210
spinal (plate), 176, 177
Acanthias,
canals, 455
cranium, 351
muscles, 390, 394
vitelline circulation, 620
A. vulgaris, see Squalus acanthias
Acanthodians, myxopterygia, 724
Acrodus, dentition, 697
Adams, L. A.,
on Arthrodira, 184, 187, 198
Dinichthys, 121, 152, 185, 188, 189, 190
Adams-Jaekel theory, 185, 187
Agar, W. E., on Protopterus, 389
Agassiz, L., on Coccosteus, 145, 202, 208
Agnathostomata, 67, 100
Allen, G., on Heterodontidae, 707
Allis, E. P.,
on Chlamydoselachus, 268, 269, 278, 279,
290, 350, 351, 355, 356, 357, 359, 360,
362, 391, 396, 397, 398, 399, 400, 415,
416, 428, 463, 465, 474, 475, 477, 479,
480, 481, 492, 629
Heterodontus, 662
Squalus, 492
Amia, egg, cleavage lines, 725, 726
Amphibia, gills, 629
Amphioxus, 70, 357, 416
cartilage, labial, 357
thyroid, 416 :
Angarichthys, spinal (plate), 177
Angulare (plate), 175, 185
Antiarchi, 177, 180, 187, 208-209
Aorta,
Chlamydoselachus, 461-466
embryonic, 465
Heptanchus, 464
Squalus acanthias, 464, 465
Apertures, Chlamydoselachus,
abdominal, VI-v*
urethral, 443
Arches,
basibranchial,
Chlamydoselachus, 359, 361, 362, 363
Heptanchus, 363
Hexanchus, 363
basihyoid,
Chlamydoselachus, 360
branchial,
Chlamydoselachus, 358-363, 396, 420,
468, 661,662,742, 743, 744 ,746; VI
Heptanchus, 363
Heterodontus, 662, 744, 745
H. japonicus, 742, 743, 744
H. phillipi, 662
gill,
Arthrodira, 199-202, 207, 391
Chlamydoselachus, 358, 363, 420-423,
593, 595, 597, 598, 599, 600, 601, 604—
617, 623, 626
Coccosteus, 199
Dinichthys, 199, 200-202
Selachii, 391, 743
Squalus, 594, 596, 600, 601
hyoid,
Arthrodira, 207
Chlamydoselachus, 359
Dinichthys, 201
sharks, 699
hyomandibular,
Chlamydoselachus, 358
Heptanchus, 700
Heterodontidae, 662
Hybodus basanus, 701
sharks, 699, 700
mandibular,
Chlamydoselachus, 356, 396
Dinichthys, 202
Heterodontus japonicus, 662, 744, '745
neural,
Cestraciontidae, 696
Hybodontidae, 696
pharyngeal in Selachii, 743
phylogeny of, 363
visceral,
Chlamydoselachus, 356, 363, 390, 396
Heptanchus, 356
Hexanchus, 356
nerves, origin of, 399
Scyllium canicula, 476
Torpedo, 743
Armor,
Antiarchi, ventral, 209
Arthrodira,
head, 122-126, 208
ventral, 198, 201
Chondrostei, head, 204
Dinichthys,
dorsal, 117, 119, 120, 125, 160-170
head, 117, 125, 127-152, 153-159, 185-
188, 189-192, 205; IV-1—IV-n1
ventral, 119, 120, 125, 170-174, 175,
180, 188, 189, 191, 192, 200
Macropetalichthys, 204, 206
Rhynchodontus, 203
Armor plates, see Arthrodira, Coccosteus,
Dinichthys
Arterial ring,
Chlamydoselachus, 617-622, 749
Heterodontus japonicus, 749
Pristiurus, 618, 748-749
Arteries,
Bdellostoma, 90
Chlamydoselachus, 461-471, 603, 617-621
Elasmobranchii, 471
Heptanchus, 467-468
Heterodontus japonicus, 749, '750, 751, 752;
VIIL-v, Villbvi
Notorhynchus, 468
vitelline, see Heterodontus and Pristiurus
below
Atterioles, Chlamydoselachus, 749, 751
Arthrodira,
arch, gill, 199-202, 207
hyoid, 207
armor, head, 122-126, 208
ventral, 198, 201
armor plates,
antero-ventro-lateral, 172
post-marginal, 134, 135
post-sub-orbital 202
spinal, 176, 179
canal, sensory, 122, 126, 135-137, 139
dentition, 146, 206, 207
fins, 195, 197-198, 200
pectoral, 197, 198, 200
gill, 210
girdle, pelvic, 197, 198
head, 180, 200, 204, 205, 218
jaw, 145, 184-185, 187, 207
mouth, 187-192
muscles, 194
neurocranium, 192-194
phylogeny, 202-211
reconstruction, 122, 123, 142
Asterolepida, 132, 179, 180, 208
Ayers, H.,
on Bdellostoma, 77, 92
Chlamydoselachus, 352, 459, 461, 463,
467, 471
*Since the plates of each article are numbered consecutively they are herein referred to by designations indicating both articles and plates.
Thus, V-11, means Article five, Plate two.
785
786
Balfour, F. M.,
on Elasmobranchs, 582
fin-fold theory, 341
Pristiurus, 589, 617, 619, 748-749
Selachii, 455
Barnhart, P.S., on Heterodontus francisci, 708,
710, 712, 713, 718
Bdellostoma, 43-62, Il1, In; 63-110,
WI-1—Il1v
artery, 90
bibliography, 101-102
distribution, 80-83, 97-98
hermaphroditism, 67, 69
longevity, 92
reproductive system, 69, 83-88, 90, 95;
I4—illiv
sex, 70, 77-78
testis, '70, 83-85, 87, II4
Bdellostoma burgeri,
distribution, 80
eggs, 86, 87, 89, 95, 97, Ilan
embryos, 68, 97
hermaphroditism, 67, 77, 82, 85, 86, 89, 95,
96, 98
ovaries, 86, 88, 89, 91, 92; II1-4
reproductive system, 76, 83-88, 90, 95;
IWa—tll-iv
size, 82, 98
testis, II]-1
Bdellostoma forsteri,
distribution, 77
hermaphroditism, 76-78
Bdellostoma stouti,
brain, 99
breeding season, 94, 95
corpora lutea, 89, 92, 95
distribution, 79, 83
egg, 47-62, 84, 85, 86, 87, 88; Il, In
blastoderm (disc), 54, 55
blastomeres, 52, 53, 54, 55, 56
blastopore, 56
capsule (shell), 49, 50, 51
anchor filaments, 50, 51
micropylar canal, 51, 52
operculum, 49, 50, 51, 62
cleavage, 47-57; I+, In
furrow, 52, 53, 55
pattern, 53, 54, 55
fertilization, 51, 85
gastrulation, 56, 302
germinal area, 47
disc, 47, 50, 52, 56, 57; I, lar
hillock, 50, 52, 54, 56, 57; I1
granulosa, 51
growth, 88-92
meroblastic, 47
micromeres, 55, 56
reconstruction, 47
segmentation, 47-57; Ia, In
embryos, 51, 57, 97, 98, 99
Bashford Dean Memorial Volume
eye, 99
hermaphroditism, 77-78, 83
mesonephros, 90, 98
mesorchia, 70, 78, 83, 84
myxopterygia, 92
ovarian follicle, 49, 51
reproductive system, 83-88, 90, 95; Wa—
Ilav
size, 79, 83, 85
spawning, 92-97
Beebe, W. and Tee-Van, J., on H. quoyi,
676
Bertrand, L., on Chlamydoselachus, 255, 265,
266, 273, 294
Bibliographies,
Bdellostoma, 101-102
Chlamydoselachus,
631-633
Dean, 23-34
Dinichthys, 213-224
Heterodontus, 764-770.
Blainville, H. M., on Heterodontus, 658, 659,
664
Blastoderm (blastodisc),
Bdellostoma, 54, 55
Chlamydoselachus, 582, 583, 584, 585, 617,
618, 620
Elasmobranchii, 582
Ginglymostoma, 582, 585, 590
Heterodontus japonicus, 582, '722, 729, 730,
731, 732, 733, 734, 738, 739, 741, 748,
749; VIIa, Villy, VII-v
H. phillipi, 582, 723, 731, 732, 733, 737,
738
Pristiurus, 582, 589, 748, 749
Scyllium, 729
Squalus, 585, 733
Torpedo, 733, 739
Blastodisc, see Blastoderm above
Blastomeres,
Bdellostoma, 52, 53, 54, 55, 56, 725
Heterodontus, 725, 278, 729, 730, 731, 732
Blastopore,
Bdellostoma, 56
Chlamydoselachus, 618
Cryptobranchus, 739
316-319; 498-505;
Ginglymostoma, 560 a
Heterodontus japonicus, 726, 738-740, 748,
749; VIIL-v
Pristiurus, 748, 749
yolk,
Chlamydoselachus, 618
Heterodontus japonicus, 739, 740, 749,
750; VIL-v
Pristiurus, 618, 748
Blastula,
Chlamydoselachus, 539, 573, 582-588
Elasmobranchii, 582
Heterodontus, 79, 712, 717, 719, 729, 731,
732, 733, 735, 736, 737, 738
Pristiurus, '731
Torpedo, 731
Bolau, H., on Chlamydoselachus, 540
Bolivar, I., on Chlamydoselachus, 255, 265,
291, 294
Borcea, J., on Scyllium, 447
Bothriolepis, 199
Brain,
Bdellostoma, 99
Chlamydoselachus, 473-475, 593-595, 597-
600; VI-—VIL-v
Heptanchus, 474-475
Heterodontus, 735, 740, 741, 742, 744, 745
Necturus, 99
Branson, E. B., on Dinichthys, 119, 120, 135,
142, 143
Braus, H., on Chlamydoselachus, 283, 342,
350, 370, 376, 386, 483, 486
Breathing valve,
Chlamydoselachus, 269-270, 420; V-1v,
Vv
Heterodontus, 735
Breeding habits,
Bdellostoma, 92-97
Chlamydoselachus, 301-302, 535
Ginglymostoma, 533-534
Heterodontus galeatus, 713
H. japonicus, '712—715, 716, 718
H. phillipi, 712-713, 715
Breeding season,
Bdellostoma, 94, 95
Chlamydoselachus, 298-302, 534
Heterodontus, 711-712, 713, 717
Brevoort, J. C., on Heterodontus japonicus,
666, 688, 689, 690, 691, 692, 756
Bridge, T. W., on Heterodontus, 202, 659,
660, 661
Brohmer, P., on Chlamydoselachus, 476, 478-
479, 482, 483, 592, 596, 627
Broili, F.,
on Acanthaspida, 177, 198, 199, 200
Gemundia, 188
Bryant, H.,
on Coccosteus, 198, 199, 200
Dinichthys, 121, 135, 151, 159, 168, 169
Bulldog Shark, 664, see Heterodontus phillipi
Bullhead Sharks, 660-661, see Herodontidae
Canal,
haversian, 146, 157
head in Chlamydoselachus, 287-290
hypobranchial, 359-362, 364
micropylar in Chlamydoselachus, 51, 52
nasal in elasmobranchs, 195
neurenteric in Heterodontus japonicus, 745
olfactory in Dinichthys, 195
pericardio-peritoneal,
Acanthias, 455
Chlamydoselachus, 455-457
Raja, 455
Canal—pericardio-peritoneal—(continued)
Scyllium, 455
Selachii, 455
Squalus, 455
sensory,
Arthrodira, 122, 126, 133-137, 139
Chlamydoselachus, 204, 205, 208, 209,
210, 266, 287-290, 294, 489-492, 606,
607, 608, 609, 611, 612, 613, 614, 615,
617, 623, 624, 625, 626, 717; Vivir
Ctenacanthus clarkii, 490
Dinichthys, 126, 133, 134, 135, 136, 142
Heptanchus, 490, 492
Heterodontus japonicus, 743, 747
Macropetalichthys, 206
Mustelus, 492
Notidanidae, 490
Placodermata, 209, 210, 211
Raja, 455
Squalus, 489-490, 492
spiracular,
Chlamydoselachus, 426-427, 744
Heterodontus japonicus, 759
Capsule, auditory, 699, 700
see also Egg, capsule
Carapace,
body,
Acanthaspida, 179, 210
Antiarchi, 208-210
Arthrodira, 198, 201
Asterolepida, 132, 208-209
Coccosteus, 175, 198, 210, 211
Dinichthys, 119, 120, 125, 160-174, 175,
180, 188, 189, 191, 192, 200
Macropetalichthys, 206
Pholidosteus, 176
central,
Dinichthys, 123, 129, 130, 132, 133, 135,
136, 141, 205
dorsal,
Dinichthys, 117, 119, 120, 125, 160-170
head,
Asterolepis, 132
Coccosteus, 134, 141, 211
Dinichthys, 127-152, 153-159, 185-188,
189-192, 205; [V-1—IV-m
ventral,
Dinichthys, 119, 120, 125, 170-174, 175,
180, 188, 189, 191, 192, 200
Carcharhinus obscurus, ovaries and oviducts,
564, 565
Carcharhinus platyodon, 565
Carcharodon rondeletii, egg and embryo, 575,
576, 577
Cartilage, in Chlamydoselachus, q.v.
Centracion, 658-659, see Heterodontus
Centraciontidae, 662, see Heterodontidae
Centrophorus, 351
Cephalaspidae, 176
Cephaloscyllium umbratile, 409
Analytical Subject Index
Cestracion, 658-659, see Heterodontus
C. francisci, see Heterodontus francisci
C. pantherinus, see Heterodontus quoyi
C. phillipi, see Heterodontus phillipi
C. quoyi, see Heterodontus quoyi
Cestraciontidae, 651, 699, '702, see Hetero-
dontidae
affinities, 694-702
arches, neural, 696
dentition, 695, 696
embryology, 651
fins, 695-696
jaw, 699
palatoquadrate, 695-696
spine, dorsal, 696
tail, 696
Cetorhinus, mouth, 277, 304, 339
Chimaera, egg, 709, 724
Chlamydoselachidae, 247-314, 663
Chlamydoselachus anguineus, 243-330; V1—
V-v; 331-520; VI1—VI-vu; 521-
646; VII1—VII-vi
aorta, dorsal, 461-466
arches,
basibranchial, 359, 361, 362
basihyoid, 360
branchial, 358-363, 396, 420, 468, 661,
662, 742, 743, 744, 746; Vian
gills, 358-363, 396, 420-423, 466-467,
593, 597, 598, 599, 600, 601, 602,
604-617, 623, 626
hyoid, 359
hyomandibular, 358
labial, 398
mandibular, 356
visceral, 356, 363, 390, 396
arteries, 461-471
embryonic, 603, 617-621
bibliography, 316-319; 498-505; 631-633
blood-vessels, 457-472
body cavity, 434, 435, 447
body form, 281-290, 336-338, 625
brain, 473-475; VIau, VIav, VI-vi
embryonic, 593-595, 597-600
breathing valve, 269-270, 275, 420; V-1v,
Vv
breeding, 298, 301
breeding season, 299, 302, 534
bursa entiana, 406-407, 412
canals,
head, 287-290
hypobranchial, 359, 360, 361, 362,
364
micropylar, 52
pericardio-peritoneal, 455-457
sensory, 204, 205, 208, 209, 210, 266,
287-290, 294, 489-492, 606, 607, 608,
609, 611, 612, 614, 615, 617, 623, 624,
625, 626, 717; Vivir
spiracular, 426-427, 744
787
cartilage,
dorsal, 369
hyomandibular, 424, 426
labial, 269, 357; VI-n
mandibular, 429
Meckel’s, 356, 358
ventral, 369
ceratohyoids, 358-359
cenogenetic characters, 497
chorda tympani, 482
cloaca and cloacal openings, 282, 285-286,
290, 293, 300, 301, 410, 411, 431, 432,
433, 434, 435, 440, 441, 450-454, 531,
532, 542, 562-563, 593-595, 610-612,
623, 624; V-v; Vi-v
colon, 410, 411, 412
color, 265-266
cranium, 309, 310, 350-356, 390, 493;
Via, Vin
denticles,
dermal, 285, 286, 287, 342-350, 623
pharyngeal, 402
dentition, 248, 249, 253, 260, 267, 271-
277, 305-311, 312, 313-314, 342-350,
591, 623, 624, 760-763; V-11—V-v
cusps, 346-349
embryonic, 274, 591
digestive system, 401-419
discovery, 248
distribution, 249-258, 264, 265, 291, 294,
303, 304, 495
ducts,
deferens, 450; VI-1v, Vi-v
mesonephric, 434, 437, 438, 439, 440,
441, 442-444, 450
duodenum, 406
ear, 355, 487-488
egg, 250, 252, 264, 299, 300, 301, 302, 303,
445, 446, 448, 531, 532, 533, 541, 542,
545, 548-549, 555, 557, 558, 567-580,
626-627; VI4
blastoderm (disc), 582, 583, 584, 585,
589, 590, 617, 618, 620
blastopore, 618
blastula, 539, 573, 582-588
capsule, 531, 560, 566-573, 578-579,
603; VII-4
tendrilliform processes, 581
case, 301, 560, 620
cleavage, 584, 585, 587
ovarian, 548-549, 623
shell, 300, 523, 538, 545
size of, 302, 303, 445, 446, 448, 544, 548,
567-574
wind, 545, 557, 568, 570, 571, 572; VIL-v
yolk,
attached, 300, 530, 627; VII-m
cord, 301; VII
mass, 300, 301, 303, 449, 533, 555-557,
559, 571, 572, 575; Vln
788
Chlamydoselachus anguineus—yolk—(contd.)
sac, 300, 301, 303, 449, 533, 555-557,
559, 571, 575, 576, 595, 596, 602, 603,
610, 612-621, 627; VIL-n
stalk, 593, 595, 597, 602, 603, 605, 610,
612, 614, 615, 618-621; VIIa
vascular (vitelline) system, 614, 617—
622, 751; VILv
embryos (embryology), 48, 250, 252, 257,
275, 277, 288, 291, 296, 298-300, 302,
303, 382, 383, 463, 468, 478-479, 483,
528, 529, 530, 555-557, 561, 573-574,
576, 581-621; VIIm—VII-v
brain, 593-595, 597-600
circulatory system, 465, 603, 606, 614,
617-622, 751; VILv
dentition, 274, 591
digestive system, 411-412, 415, 419
eye, see below
fins, see below
folds, 608, 611, 623-625
food, 561, 626-627
gastrulation, 539, 570, 585, 588-590
gills, see below
mouth, 593-597, 599-602, 604, 605,
607-616; VII-n, VII-m
myomeres, 382, 383, 388, 593, 624
nasal opening, 293, 599, 600-602, 604,
607-617; VILu, VIlm
nerves, 478-479, 483
on egg; VIL-v
size, 302, 393, 555, 556, 559-562, 573-
574, 578
somites, 388
spiracles, 279-281, 340, 423-430, 506,
598, 599, 600, 601, 602, 604, 607, 608,
610-613, 615; V-m
esophagus, 402-403
evolution, anatomical, 492-495
eye, 277-278; V-11
embryonic, 277, 355, 593, 594, 597, 599,
600-602, 604-608, 610, 611, 612, 613,
614, 623, 625
muscles, 391-394, 478; VI-1v
lid, 278, 314
fins, 260, 291-297, 314, 340-342
anal, 280, 291, 303, 304, 364, 380
embryonic, 602, 604,608,610-615,623
caudal, 280, 281, 288, 290, 293-297, 340,
380-381
embryonic, 601, 602, 608, 610-615,
617, 623-625
dorsal, 209, 281-283, 285, 288, 292-293,
340, 364, 377-379
embryonic, 595, 601, 602, 604, 608,
611-615, 617, 623
pectoral, 281, 288, 307-373
embryonic, 291, 295, 593-595, 598,
600-602, 604-605, 607-608, 611-615,
626
Bashford Dean Memorial Volume
pelvic, 291, 292, 340, 373-377, 394, 395,
434, 450, 541; V-v; Viv
embryonic, 573, 594, 595, 601, 602,
604, 607, 608, 610-612, 614-615
see also myxopterygia below
fold, maxillary, 269, 281
opercular, 281
tropeic, 281-285, 342, 385-388
embryonic, 608, 611, 623-625
follicles, ovarian, 445, 546, 549
food, 297
foramen magnum, 356
ganglion, ciliary, 478-479
Gasserian, 479, 480, 481
gestation, 302-303, 538-540, 556
gills, 306-308, 420-423; V-m
arches, 359, 463, 467, 468
blood vessels of, 420, 469-471
clefts, 422, 429-430, 468
covers, 267, 281, 304, 339-340
embryonic, 593-595, 597-602, 604-617,
623, 626-629, 758; VIla—VIL1v
external in adults, 629-630
filaments, 420-423, 429, 470, 626-630,
758, 759
slits, 266, 314, 371-373; VI-v
girdle,
pectoral, 370-373
pelvic, 373-377; VL-v
glands,
nidamental, 432, 433, 434, 445, 446, 448,
550-552, 578
pancreatic. 413-415
rectal, 410-411
thyroid, 415-418
glomeruli, 437
head, 266-280, 396, 606, 625-626; V-u,
Van
heart, 457-461
intestine, valvular, 408-409; VI1v
jaw, 268, 269, 272, 281, 353, 354, 356, 358,
484
liver, 412-413
mating, 301 5
membranous labyrinth, 487-488; Vv
mesentery, 437, 438, 439, 440, 442, 443,
445, 447
mesonephros, 432, 433, 434-438
tubules of, 437
mouth, 267-269, 295, 338-339, 623, 625;
VA
embryonic, 593-597, 599-602, 604, 605,
607-616, 623-625
muscle bundle, 484, 485
muscles, 381-400; VL-1v
appendicular, 381, 394, 395
axial, 382-394
branchiomeric, 396-400
embryonic, 382, 394
eye, 355, 391-394, 478; VIiv
hypobranchial, 388-391
intermandibular, 399-400
innervation of, 399
keel, 387-389
metameric, 391-395
m. rectus abdominalis, 387-389
m. rectus profundis, 387-389
myxopterygial, 395
pharyngeal, 397
tail and trunk, 382-391
ventrolateral, 384-385
myxopterygia, 291-292, 295, 298, 373,
376-377, 395, 451, 452, 453, 454, 472,
541-542, 624; V-v; VL-v
nasal organs, 207, 279, 503, 593, 599, 600-
602, 604, 607-617
nerves, 472-487; VI-vi
chorda tympani, 482
nervus collector, 486-487
cranial, 475-485; VI-vu
facial, 482
fifth, 481
glossopharyngeal, 482
occipital, 483-485
oculomotor, 479-480
optic, 477
seventh, 481
spinal, 368, 485-487
trigeminal, 478, 480-481
vagus, 482-484
embryonic, 483
neurocranium, 350
nomenclature, 303-305
colloquial, 304-305
notochord, 351, 352, 363-370, 492
ovaries, 299, 432, 433, 445-446, 447, 535,
543, 544-547
oviduct, 299, 302, 431, 432, 433, 434, 435,
437, 445, 446-450, 543, 544, 549-550,
558, 559, 562, 563
oviparity, 300, 301, 531-533, 578, 579,
580
ovoviparity, 580
palatoquadrate 353-354, 355, 356, 358,
424-425
papilla, urethral and urinary, 431, 432, 433
parasites, 298
pelvis, 373-376; VI-v
pharynx, 397, 402
phylogeny, 305-311, 314-315, 492-495
pit organs, 288-290
placenta, 301
pores,
abdominal 285-286, 432, 434, 435, 440,
450, 453, 454 455; V-v
head, 289-290
urethral, 432. 433, 439, 440, 441, 442
pylorus, 405-406
vestibule of, 404-405, 412
radials, 376, 377, 378, 379, 380, 381
Chlamydoselachus anguineus—(continued)
raphe, 571, 572
rectum, 410-412
reproductive system, 412, 431-455, 541-
564; VI-v
respiratory system, 267, 279-281, 339-
340, 359, 419-430, 466-471, 593-
595, 596, 597-602, 604-617, 625-630,
758, 759; VIla1—VIL-i1v
scales, 286, 287, 288, 294, 342-350
sense organs, 487-492
sinus,
urinary, 438-441, 442, 443
urogenital, 431-434, 438, 439, 440, 450
size, 248, 252, 254, 255, 260-265, 273, 274,
279, 281, 282, 283, 290, 295, 444, 546,
577, 578, 662, 663
skeleton, 350-380, 494
visceral, 355, 356-364, 390; VI-u, Vian
spawning habits, 301, 302, 535
spleen, 418-419
stomach (cardiac), 403-404, 412
tail, 248, 249, 250, 288, 289, 290-291, 293,
364, 369-370, 624-625
embryonic, 296, 593, 594, 598, 601, 604,
607, 611-614, 617, 620-621
fin, 450
testes, 450
tongue, 270; V-u1
tubules, collecting, 437, 442-444
urethral aperture, 432, 441, 442, 448
uterus, 432, 433, 439, 443, 446, 447, 449,
535, 536, 548, 552-562
venous system, 471-472
embryonic, 603, 618-622
vitelline, 614, 617-622, 751
vertebral column, 363, 366, 367, 368-370,
436; Via, Via
viviparity, 298-301, 528, 531-534, 542,
559
yolk,
attached, 300, 530, 627; VIL
cord, 301; VII-
mass, 300, 301, 303, 449, 533, 555-557,
559, 571, 572, 575; Vila
sac, 300, 301, 303, 449, 533, 555-557,
559, 571, 575, 576, 595, 596, 602, 603,
610, 612-621, 627; VIL
stalk, 593, 595, 597, 602, 603, 605, 610,
612, 614, 615, 618-621; VII 1
vascular (vitelline) system, 614, 617-
622, 751; VIL-v
young, 300
Chlamydoselachus lawleyi, 311-313, 348, 349,
495
C. tobleri, 313-314, 348
Chondrostei, 204
Circulatory system,
Acanthias, vitelline, 620
Chlamydoselachus, 461-472, 603, 614,
Analytical Subject Index
617-622, 751
Elasmobranchii, 621
Felichthys, 622
Heterodontus japonicus, 739, 742, 743, 744,
748, 749, 750, 751, 752, 753, 755, 756;
VIIL-vir
Pristiurus, vitelline, 618, 748-749
Squalus, vitelline, 620
Cladodus, 306, 311, 372, 373, 495
dentition, 308-309
C. acutus, 308, 348, 349, 350
dentition, 348, 349, 350
C. mirabilis, 308
C. neilsoni, fin, 372, 373
Cladoselache, 9-10, 341, 375, 376
dentition, 348, 349, 350
dermal denticles, 347
fin, 375
myxopterygia, 724
Clark, J. M., on Dinichthys, 119
Clavicular (plate), 117, 119-120, 160, 166,
175, 177, 179, 185
Claypole, E. W.,
on Arthrodira, 126, 127
Dinichthys, 117, 118, 135, 142, 145, 152,
160, 166, 176, 195
Cleavage, see Egg, cleavage
Cloaca,
Chlamydoselachus, 282, 285-286, 290, 293,
300, 301, 410, 411, 431, 432, 433, 434,
435, 440, 441, 450-454, 531, 532, 542,
562-563, 593-595, 610-612, 623, 624;
V-v; Viv
Elasmobranchii, 549
Ginglymostoma, 530
Heterodontus, 713
Coccosteus, 144, 158, 168, 175, 180, 184, 188,
202, 211
armor, 134, 141, 175, 198, 210, 211
armor plates,
antero-dorso-lateral, 199
antero-lateral, 199
post-marginal, 134
post-sub-orbital, 143, 199
postero-dorso-lateral, 199
postero-lateral, 199
spinal, 176, 177, 210
dentition, 145
gill arches, 199
head, 211
jaw, 185, 187
muscles, 190
vertebral column, 196, 197
C. angustus, 198, 200
C. birkensis, 176
C. decipiens, 127, 134, 136, 143, 144, 168,
176, 177
Collections,
Bdellostoma, 48
Chlamydoselachus,
789
American Museum, 254, 255, 258-259,
266, 291, 335, 403, 420, 489, 529, 625,
626, 630
Columbia University, 529, 548, 570,
571, 579, 638
Museum of Comparative Zoology, 569,
609, 610
von Rautenfeld, 596
White, 335
Dinichthys,
American Museum, 116, 141, 143, 146,
151, 169, 174, 177, 197
Buffalo, 134, 135, 151, 169, 170, 174,
177, 190, 197
Bungart, 169
Cleveland, 115-116
Jaekel, 175
Museum of Comparative Zoology, 174
Heterodontidae,
American Museum, 654, 678, 684, 693,
702, 756
Collett, R., on Chlamydoselachus, 254, 255,
267, 268, 273, 277, 279, 291, 294, 359,
403, 411, 413, 415, 437, 447-448, 541,
544, 545, 557, 558, 630
Color pattern,
Chlamydoselachus, 265, 266
Gyropleurodus, 677
Heterodontus, 663, 669
H. francisci, 677, 681, 683, 684
H. galeatus, 687-688
H. japonicus, 692, 693, 694, 702, 747, 748,
755, 756, 757
H. phillipi, 666, 667, 668, 669
H. quoyi, 676, 677, 678, 679, 680
H. zebra, 675
Conel, A., 63-110
on Bdellostoma, 78
Myxine, 75
Cope, E. D., on Chlamydoselachus, 306-309
Corning, H. K., on Lacerta, 389
Corrington, J. D.,
on Chlamydoselachus, 464
elasmobranchs, 471
gills, 423
Cranium,
Acanthias, 351
Centrophorus, 351
Chlamydoselachus, 309, 310, 350-356, 390,
493; VI4, VIat
Elasmobranchii, 701
Heptanchus, 351, 699-700
Heterodontus, 662, 684, 699, 700, 701
Hybodus, 699, 700, 701
Scyllium, 699, 700
Scymnus, 351
shark, 699
Synechodus, 701
Crested Shark, 687, see Heterodontus galeatus
Crossopterygii, 629
790
Cryptobranchus, 722, 728, 739
Ctenacanthus clarkii, 348, 349, 350, 373, 490
dentition, 348, 349, 350.
fins, 373
Cunningham, J. J., on Myxine, 70, 71, 72, 73,
75, 76, 77, 91, 92, 93
Cuvier, G. C. L., 568, 659, 664
Cyclostomes, 97, 99, 209
Daniel, J. F.,
on Chlamydoselachus, 382, 395, 485
Elasmobranchii, 336, 345, 347, 351, 358,
363, 366, 370, 374, 389
Galeus, 405
Heptanchus, 403, 407, 409, 411, 415,
418, 441, 444, 446, 449, 474-475, 483,
484, 492
Heterodontus, 661, 663, 681, 684, 696,
699-700, 703, 707,
muscles, 394
Notidanus, 490
spiracles, 427
Squalus, 444
Torpedo, 484
Darbyshire, A. D., on Squatina, 427
Dasyatis, ovaries and oviduct, 566
Davidson, P., on Heptanchus, 389, 391, 393,
395, 396
Davis, J. W., on Cladodus (teeth), 309, 310
Dean, B.,
bibliography, 23-34
biography, 1-22; 35-42; 7 portraits
Bdellostoma,
original drawings, 83, 86, 87, 89; Il4,
IL-n; W14—II1v
original notes, 48, 68, 80, 81, 82, 83, 85,
94, 95, 96, 97, 98
Chlamydoselachus,
original drawings, 247, 526, 529, 531,
539, 554, 568, 571, 572, 573, 576, 578,
583, 587, 588-589, 590, 592-616, 618,
626; VII1—VIIv1
original notes, 247, 250-252, 257, 258,
262, 265, 280, 297, 300-301, 302, 303,
525, 535, 536, 543,-546, 548, 549, 555,
556, 558, 570, 583, 584, 588-589, 590,
592
Heterodontus japonicus,
original drawings, 655-656, 704, 714,
715, 719, 720, 721, 729, 730, '732,
733-734, 737, 738, 739, 740, 745, 746,
747, 748, 749-752, 753-755, 756, 760,
762
original notes, 651-652, 653, 654, 656,
657, 689, 702, 703-705, 708, 710-712,
713, 717, 718, 719, 721, 722, 724-728,
752, 753-755, 756
on Amia, 725
Arthrodira, 125, 145, 180
Bdellostoma, 11, 12, 47, 51, 55, 56, 78,
Bashford Dean Memorial Volume
79, 86, 87, 88, 89, 90, 91, 92, 99
Chlamydoselachus, 250, 475, 526, 527,
528, 533, 546, 574, 585
Chimaera, 709, 724
Cladoselache, 9-10, 349, 375, 376
Triakis semifasciatus, 345
tubercles, 210
Didymodus, 306-309
Dinichthys,
arches,
Coccosteus, 175
Ctenacanthus, 490
Cyclostomes, 97, 98
Dinichthys, 117, 118, 119, 120-121, 145,
160, 166, 169, 1°70, 173, 174, 184, 196
embryology, 10
fin-fold theory, 342
fins, origin of paired, 9-10
Heptanchus, 338
Myxinoidea, 67-69, 97-100
Ostracoderms, 99
Palaeospondylus, 11
Placoderms, 9
Deinega, W. A., on Chlamydoselachus, 350,
351, 360, 370, 371, 373, 380, 413, 415,
419, 449, 553, 562, 563
Denticles,
dermal,
Chlamydoselachus, 285, 286, 287, 342—
350, 623
Cladoselache, 347
Heterodontus, 747, 755, 760
pharyngeal, 402
Dentition,
Acrodus, 697
analogy to scales, 344-347
Arthrodira, 146, 206, 207
Cestraciontidae, 695, 696
Chlamydoselachus, 248, 249, 253, 260, 267,
269, 271-277, 305-311, 313-314,
343-350, 591, 623, 624, 760-763;
Viu—V-v
Cladodus, 308-310, 348, 349, 350
Chladoselache, 348, 349, 350
Coccosteus, 145
Ctenacanthus, 348, 349, 350
Didymodus, 306
Dinichthys, 145-146, 184, 186, 187, 188,
190, 211
Heptanchus, 270, 311, 347
Heterodontus, 662, 698
H. francisci, 684
H. galeatus, 687, 688
H. japonicus, 691, 694, 711, 759, 760-763
H. phillipi, 666, 670-675, 681
H. quoyi, 680-681
H. zebra, 676
Hybodontidae, 348, 349, 696, 697
Jagorina, 206
Mylostoma, 186
Notidanidae, 673
Paleospinax, 698
phylogenetic significance, 347-348
Pleuracanthus laevissimus, 310
Synechodus, 697-698
gill, 199
hyoid, 201
armor,
connecting, 179-192
dorsal, 117, 119, 120, 125, 160-170
head, 117, 125, 127-152, 153-159, 185-
192, 205; IV1—IV-11
ventral, 119, 120, 125, 170-174, 175,
180, 188, 189, 191, 192, 200
armor plates,
antero-dorso-lateral, 117, 118, 119, 124,
162, 163-165, 168, 180, 182, 183, 184,
204, 211
antero-lateral, 124, 125, 165, 166-169,
170, 171, 174, 177, 178, 179, 182, 190,
191, 192, 200, 201
antero-median-ventral, 123, 125, 126,
172, 173-174, 191, 192, 201
antero-supra-gnathal, 123, 125, 145,
146-147, 149, 153, 160, 190, 207
antero-ventro-lateral, 125, 126, 171, 172,
173, 175, 177, 178, 185, 211
central, 123, 125, 128, 132, 135-136,
160, 161
clavicular, see antero-lateral above
externo-basal, 123, 128, 129, 133-135,
160, 161, 181, 184,
infero-gnathal, 123, 125, 148-150, 153,
160, 186; [V-vir
interno-lateral, 124, 125, 126, 169, 175—-
179; [V-vint
marginal, 120, 123, 125, 128, 132, 133-
134, 135, 160, 161; [V-m
median-basal, 123, 125, 128, 132, 133,
160, 161
median-dorsal, 118, 124, 125, 160-163,
170, 178, 179, 184, 188, 191, 200, 201
median-ventral, 125, 126, 172, 173, 192
pineal, 123, 128, 132, 137, 160, 196
post-marginal, 123, 125, 128, 132, 134-
135, 160, 161, 192
post-maxillary, 117, 118, 119
post-nasal, 123, 125, 139, 141-143, 153,
158, 160, 192; IV-11
post-orbital, 123, 125, 132, 136, 141,
143-146, 160, 161,
post-sub-orbital, 123, 125, 143-146, 150,
153, 158, 159, 160, 187, 190, 191, 192,
200, 207, 211; [V-iv
post-supra-gnathal, 153
postero-dorso-lateral, 119, 124, 125, 159,
165-166, 169, 170, 177, 204
postero-infero-gnathal, 123, 125, 150-
152, 153, 184, 192, 208; IV-vir
postero-lateral, 120, 124, 125, 169-170,
Dinichthys—armor—postero-lateral—(contd.)
177, 192, 199; IV-vir
postero-supra-gnathal, 123, 125, 145,
147-148, 153, 160, 186
postero-ventro-lateral, 125, 126, 172,
173, 204
pre-nasal, 158
pre-orbital, 123, 125, 128, 132, 139, 141,
142, 157, 158, 160, 161, 205
rostral, 123, 125, 132, 137, 141, 157,
158, 160, 161
spinal, 124, 125, 126, 159-179, 197, 198;
TV-1x
sub-orbital, 118, 119, 123, 125, 138-141,
142, 143, 153, 157, 158, 160, 191, 200,
205, 211
bibliography, 213-224
branchial shield, 199
canals,
olfactory, 195
sensory, 126, 133, 134, 135, 136, 142
condyle, 163, 164, 180, 181, 182, 188, 192,
196
dentition, 145, 146° 184, 186, 187, 188,
190, 211
fins and fin rays, 197-199, 202
fontanelle, 117
food, 202
fossa glenoidalis, 180, 181, 182
gills, 199, 200-202
arches, 199
gnathal elements, 122, 183-187, 192, 207,
209, 210, 211; IV-v—IV-v1
head, 127-159, 189, 193, 194, 195, 211;
IVi—IV-m
history, 115
jaws, 118, 121, 138-155, 184, 185, 187,
188, 189, 190, 191,
mandible, 121, 148, 184, 185; [V-vir
maxilla, 121, 122, 144, 152
movements, 158, 189, 192
muscles, 187-192
premaxilla, 122
mouth, 187
muscles, 188, 189-191
jaw, 187-192
m. adductor mandibuli, 190
m. depressores capitis, 190-191
m. depressores gnathalis, 191
m. levatores capitis, 189-190
m. levatores gnathalis, 191
neurocranium, 192-196
orbit, 118, 128, 157, 161
phylogeny, 192, 194, 202-213
pineal organ, 141, 196
plastron, 170-174
quadrate, see armor plates, post-sub-
orbital above
reconstructions, 117-122, 142, 143,145, 152,
160, 161, 166, 168, 169, 174, 202, 203
Analytical Subject Index
body, 180, 188, 189, 192
head, 153-159, 191, 192
sclerotic ring, 158-159
skeleton, 192, 199
spine, pectoral, 198
vertebral column, 196-199
Dinichthys curtus, 197; [V-vut
D. intermedius, 133, 150, 154, 159, 169, 175;
1V-3—1V-10, [V-vu, [V-1x
D. lincolni, 207
D. magnificus, 121, 159, 168
D. mirabilis, 121
D. terrelli, 119, 120, 122, 135, 136, 141, 142,
143, 144, 160, 173; [V-1v, 1V-vir
Dinognathus ferox, 152
Dinomylostoma, 126, 151
Diplodus, 306, see Didymodus
Dipnoi, 184, 629
Distribution,
Bdellostoma, 77, 79, 80-82, 83, 97-98
Chlamydoselachus, 249-258, 264, 265, 291,
294, 303, 304, 495
Heterodontidae, 661
Heterodontus francisci, 664, 681, 683, 709-
710
H. galeatus, 664, 686, 687
H. japonicus, 653, 654, 688-689, 709-710
H. phillipi, 664, 686, 689, 710, 712, 713
H. quoyi, 664, 676, 677
H. zebra, 664, 675, 689, 693
Myzxine, 72, 73, 75
Déderlein, L., on Chlamydoselachus, 248,
249, 278, 298
Doflein, F., on Chlamydoselachus, 253, 277,
291, 295, 296, 574
Dumeril, A.,
on Cestracion, 658, 659
Heterodontus quoyi, 677, 705
Duodenum,
Chlamydoselachus, 406
Heptanchus, 407
Eastman, C. R.,
on Arthrodira, 180, 187, 202
Dinichthys, 118, 119, 135, 160, 166, 169,
170, 173, 175
Macropetalichthys, 204
Orodus, 697
Echeneis, 357
Edgeworth, F. H., on Scyllium, 389
Egg,
Amia, 725, 726
Bdellostoma, 47-61, 86, 87, 88-91, 95, 97;
Ia—tIlan
B. burgeri, 86, 87, 89, 95, 97; UW1-
B. stouti, 47-62, 84, 85, 86, 87
blastoderm (blastodisc),
Bdellostoma, 54, 55
Chlamydoselachus, 582, 583, 584, 585,
617, 618, 620
791
Elasmobranchii, 582
Ginglymostoma, 582, 585, 590
Heterodontus japonicus, 582, 722, 729,
730, 731, 732, 733, 734, 738, 739, 741,
748, 749; VIlI4, VIllav, VIIL-v
H. phillipi, 582, 723, 731, 732, 733, 737,
738
Pristiurus, 582, 589, 748, 749
Scyllium, 729
Squalus, 585, 733
Torpedo, 733, 739
blastomeres,
Bdellostoma, 52, 53, 54, 55, 56, 725,
Heterodontus, 725, 728, 729, 730, 731,
732
blastopore,
Bdellostoma, 56
Chlamydoselachus, 618
Cryptobranchus, 739
Ginglymostoma, 560
Heterodontus japonicus, 726, 738-740,
748, 749; VIL-v
Pristiurus, 748, 749
yolk,
Chlamydoselachus, 618
Heterodontus japonicus, 739, 740,
749, 750; VIII-v
Pristiurus, 618, 748
blastula,
Chlamydoselachus, 539, 573, 582-588
Elasmobranchii, 582
Heterodontus, 712, 719, 729, 731, 732,
733, 735, 736, 737, 738
Pristiurus, 731
Torpedo, 731
capsule,
Bdellostoma, 49, 50, 51
Carcharodon, 575, 576, 577
Chimaera, 709
Chlamydoselachus, 531, 560, 561, 566-
573, 578, 579, 603; VIL1
Ginglymostoma, 530, 558, 560, 561, 568,
576-577, 579, 580-581
Heterodontus francisci, 707-708
H. galeatus, 706-707, 715
H. japonicus, 705, 707-709, 712, 713-
714, 715, 717, 720, 727, 752, 753;
Vill-vu
H. phillipi, 705-707, 712, 713, 723
see also case, shell and tendrilliform
processes below
Carcharhinus, 564
Carcharodon, 207, 575, 576, 577
case,
Cestracion, 584, 585
Chimaera, 709, 724
Chlamydoselachus, 300, 301, 560, 620
Ginglymostoma, 560
Chlamydoselachus, 250, 252, 264, 299, 300,
301, 302, 303, 445, 446, 448, 531, 532,
792
Egg—Chlamydoselachus—(continued)
533, 541, 542, 545, 548, 555, 557, 558,
566-680; VII4, VILv
cleavage,
Amia, 725, 726
Bdellostoma, 47, 51-57; Il1, In
Cestracion, 584, 585
Chimaera, 724
Chlamydoselachus, 584, 585, 587
Cryptobranchus, 728, 729
discoidal, 51, 728-732
furrows, 52, 53, 55, 739; VIIl4
Heterodontus, 584, 653, 656, 716, 722,
724-732, 739, 749; VIll4, VIlL-vn
holoblastic, 724-725, 727, 748
Lepidosteus, 726, 728
lines, 47, 584, 585, 725-728, 731, 732
Necturus, 726
pattern, 53, 54, 55
Pristiurus, 589
Scyllium, 729
Cryptobranchus, 728
Elasmobranchii, 545, 578, 582, 709
Galeocerdo, 564
gastrulation, |
Bdellostoma, 56, 302
Chlamydoselachus, 539, 570, 585, 588-
590
Heterodontus japonicus, 719, 720, 725
729, 732-738, 739
H. phillipi, 717, 733, 735, 736, 737,
738
Torpedo, 738
germinal disc,
Bdellostoma, 47, 50, 52, 56, 57; IL1, In
Chlamydoselachus, 589, 590
Heterodontus japonicus, 723, 725, 726, |
728, 733, 749; VIll4, VIIL1,
Villvn
H. phillipi, 723
Pristiurus, 589, 723, 727
Ginglymostoma, 301, 530, 533, 557, 558,
559, 560, 561, 564, 568, 573, 576-577,
579-581
Heterodontus francisci, 702-703, 707-708,
712
H. galeatus, '706-707, 712, 713, 715, 716
H. japonicus, 527, 584, 641, 689, 703-705, |
708-709, 712, 713-715, 716, 717, 719,
720, 722, 724-727, 728, 729, 730, 731,
732, 733, 749, 752-753; VIII,
Villa, VIILv, Vill-vn
H. phillipi, 705-707, 711, 712, 713, 723, |
731, 732 |
Homea burgeri, 48
Lamna, 574
Lepidosteus, 726, 728
Myzxine, 74, 88-91, 90
Necturus, 726
Oxyrhina, 576
Bashford Dean Memorial Volume
polarity,
Bdellostoma, 49-52
Heterodontus japonicus, 726-728
Pristiurus, 589, 723, 727
Pteroplatea maclura, 565
Scyllium, 729
segmentation, see cleavage above
shells,
Bdellostoma, 49
Chlamydoselachus, 300, 533, 538, 545
Elasmobranchii, 578
Ginglymostoma, 533, 576, 581
see also capsule and case above and
tendrilliform processes below
size,
Bdellostoma, 89, 95
Carcharodon, 575, 576
Chlamydoselachus, 302, 303, 445, 446,
448, 544, 548, 567-574
Ginglymostoma, 573
Heterodontus, 725
Lamna, 574, 575
Oxyrhina, 576
Squalus, 585
tendrilliform processes of capsule
Chlamydoselachus, 581
Ginglymostoma, 579, 581
Heterodontus galeatus, 706
Torpedo, 739
wind,
Chlamydoselachus, 545, 557, 568, 570,
571-572, 577; VILv
Ginglymostoma, 558
Pteroplatea maclura 565
yolk,
blastopore,
Cryptobranchus, 739
Heterodontus japonicus, 739, 740,
748, 749, 750; VIll1v, VIILv
cord, 301; VII-n
mass,
Chlamydoselachus, 572; VILv
Ginglymostoma, 577, 579
Heterodontus japonicus, 733, 739,
741; Vilav, VIILv
Pristiurus, 748
sac,
Chlamydoselachus, 300, 301, 303,
449, 533, 555-557, 559, 571, 573 576,
595, 596, 602, 603, 610, 612-621;
Villon
Heterodontus japonicus, 719, 746,
747, 748, 752, 756
Pristiurus, 756
Raja, 756
Spinax, 756
stalk,
Chlamydoselachus, 593, 595, 597,
602, 603, 605, 610, 612, 614, 615, 618-
621; VI-u—VII-vn
Heterodontus japonicus, 741, 744,
745, 750, 751; VULv1
Pristiurus, 748
syncytium, see Heterodontus japonicus,
periblast
vascular system,
Chlamydoselachus, 620-622; VIL-v
Felichthys, 622
Eichwald, G. E. von, on Arthrodira, 202, 208
Elasmobranchii, 201, 204, 206, 208
anatomy, 336
canal, pericardio-peritoneal, 455
capsule, nasal, 195
cartilage, labial, 357
circulatory system, 465, 471, 621
cloaca, 549
cranium, 701
eggs, 544, 545, 578, 582, 709
blastoderm (disc), 582
blastula, 582
embryos, 10, 301, 578, 582, 709
myomeres, 382
somites, 742, 743
spiracle, 342, 428
fins, 341-342
jaw, 745
muscles, 391, 394, 742, 743
appendicular, 394
embryonic, 742, 743
eye, 391, 742, 743
myxopterygia, 531
ovaries and oviducts, 301, 549, 565-566
reproductive system, 547
skeleton, 366
thyroid gland, 418
uterine mucosa, 301
vertebral column, 366
viviparity, 301
Embryos and Embryology,
Bdellostoma, 51-57, 68, 97, 98, 99
canal, sensory, see Canal above
Carcharodon rondeletii, 575-576
Cestracion, 651
Chlamydoselachus, 48, 250, 252, 257, 275,
277, 288, 291, 296, 298-300, 302, 303,
382, 383, 393, 463, 468, 478-479, 483,
528, 529, 530, 535-537, 555-562, 573-
574, 576, 581-621, 758; VIlm—VIL-v
For details see Chlamydoselachus,
embryos
circulatory system,
Chlamydoselachus, 465, 603, 614, 617-
622, 751
Felichthys felis, 622
H. japonicus, 739, 742, 743, 744, 748,
749, 750, 751, 752, 753, 755, 756;
Vill-vm
dentition,
Chlamydoselachus, 274, 591
Heterodontus japonicus, 759, 760-763
Embryos—dentition—(continued)
H. phillipi, 761, 762
ectoderm and entoderm,
Heterodontus japonicus, 734, 738, 739,
741, 742
H. phillipi, 737
elasmobranchs, 10, 301, 552, 582, 621, 742
eye,
Chlamydoselachus, 277, 355, 593-594,
597, 599, 600-602, 604, 608, 611, 612,
613, 614, 623, 625
Heterodontus japonicus, 741, 742, 743,
745, 746, 747
Felichthys felis, 622
fins,
Chlamydoselachus, 291, 295, 575, 593-
595, 598-602, 604, 605, 607, 608,
610-625, 626
Heterodontus japonicus, 740, 741, 742,
743, 744, 745, 746, 747, 748, 755
Squalus, 595, 601, 755
folds,
Chlamydoselachus, 608, 611, 623-625
Heterodontus, 734, 740, 745, 746, 747
food of embryos,
Chlamydoselachus, 561, 626-627
Ginglymostoma, 561
Ganoids, 722
gastrulation,
Bdellostoma, 56
Chlamydoselachus, 539, 570, 585, 588-
590
Heterodontus japonicus, 719, 720, 725,
729, 732-738, 739
H. phillipi, 717, 733, 735, 736, 737, 738
Torpedo, 738
gills,
Chlamydoselachus, 468, 593-595, 597-
602, 604-617, 623, 625-629, 630, 758;
VII u—VIL-v
Heterodontus japonicus, 742-747, 752,
753, 758, 759, 760; VIIL1—VIIL-
H. quoyi, 758-759
Selachii, 743
Squalus, 594, 596, 600, 627, 628, 629
Ginglymostoma, 301, 560-562
Heterodontus francisci, '718~721
H. japonicus, 527, 651, 653, 654, 662-663,
689, 693, 694, 709, 717-751, 753, 754,
758, 760-763; VUL1—VU vr
For details see H. japonicus, embryo
H. phillipi, 582, 672, 712, 716, 717, 722-
725, 731, 732, 734, 735, 736, 737, 738,
761
For details see, H. phillipi, embryo
H. quoyi, 574-575
Lamna, 574-575
mouth,
Chlamydoselachus, 593-597, 599-602,
604, 605, 607-616; VIL-n, VIL
Analytical Subject Index
Heterodontus japonicus, 745, 746, 747,
759, 760; VU, VILL
myomeres,
Chlamydoselachus, 382, 383, 388, 593,
624
Heterodontus japonicus, 744, 745, 746,
VUl-n, VIL
Squalus, 383
Myzxine, 68
nasal openings,
Chlamydoselachus, 293, 599, 600-602,
604, 607-617; VIL, VIL-u
Heterodontus japonicus, 747
nerves,
Chlamydoselachus, 478-479, 483
Spinax, 483
oxygen used by, 560, 561
Oxyrhina, 576
Pristiurus, 722, '748, 750
Scyllium, 476, 722
Selachii, 742, 743
size,
Chlamydoselachus, 302, 303, 573-576,
592-617
Heterodontus francisci, 718, 744-747
H. japonicus, 654, 720, 721, 739, 740-
742, 745-747, 759, 760, 761, 762
Lamna, 574
spiracle, :
Chlamydoselachus, 279-281, 340, 423-
430, 596, 598-602, 604, 607-608,
610-613, 615; VIL, VIlm
Elasmobranchii, 340, 428
Heterodontus francisci, 681, 683
H. japonicus, 692, 741, 742, 744, 745,
746, 747, 755, 757, 759
H. phillipi, 665, 666, 667
H. quoyi, 677, 678
Hexanchus, 428
Squalus, 487, 600
Squatina, 340, 427
Spinax, 600
Squalus, 593-595, 596, 600, 601, 627, 628,
629, 722, 734, 735, 742
tail,
Chlamydoselachus, 275
Heterodontus japonicus, 741, 742, 744,
746
Torpedo, 734
vitelline circulation,
Acanthias, 620
Chlamydoselachus, 603, 614, 617-622
Felichthys felis, 622
Heterodontus japonicus, 748, 749, 750,
752, 753, 755, 756; VUl-v, VUI-vi
Pristiurus melanostomum, 618, 748-749
Squalus, 620
Evans, H. M., on Heterodontus, 669
Evermann, B. W. and Radcliffe, L.,
on Heterodontus, 660, 676, 681
793
H. francisci, 681
H. quoyi, 676
Excretory system, see, Mesonephroi
Eycleshymer, A. C., on Lepidosteus, 728
Eye,
Bdellostoma stouti, 99
Chlamydoselachus, 277-278, 280; V-v
Heptanchus, 393
Heterodontus francisci, 677
H, japonicus, 662, 694, 741, 742, 743, 745,
746, 747
H. quoyi, 677, 679
Felichthys felis, 622
Ferguson, A. S.,
on Elasmobranchs, 418
Fins,
anal,
Cestraciontidae, 696
Chlamydoselachus, 281, 290, 291, 303,
304, 364, 380
embryonic, 602, 604, 608, 610-623
Heptanchus, 380
Heterodontus francisci, 681, 683
H. galeatus, 687-
H. japonicus, 663, 693
embryonic, 744, 745
H. quoyi, 676, 678
Hybodus, 696
caudal,
Chlamydoselachus, 280, 281, 288, 290,
293-297, 340, 380-381
embryonic, 601, 602, 608, 610-615,
617, 623-625
Coccosteus, 210
Heterodontus francisci, 681
H. japonicus, 693, 694, 744, 745, 746,
755
embryonic, 744, 745, 746, 755
H. phillipi, 666
H. quoyi, 678
dorsal,
Acanthaspis, 198
Cestraciontidae, 695, 696
Chlamydoselachus, 209, 281-283, 285,
288, 292-293, 340, 364, 377-379
embryonic, 595, 601-602, 604, 608,
611-615, 617, 623
Dinichthys, 917
glands in, 669
Heptanchus, 379
Heterodontus francisci, 663, 681, 683
H. galeatus, 687
H. japonicus, 663, 692-693
embryonic, 744, 745, 747, 748
H. phillipi, 669
H. quoyi, 678, 679
H. zebra, 676
Hybodus, 669, 696
Mustelus, 379
794
Fins—dorsal—(continued)
Squalus, 669
Elasmobranchii, 341-342
Heterodontidae, 342, 660, 663
origin of, 379
paired, 9-10, 341-342
pectoral,
Arthrodira, 197-198
Cestraciontidae, 696
Chlamydoselachus, 281, 288, 370-373
embryonic, 291, 295, 593-595, 598,
600-602, 604-605, 607-608, 611-615,
626
Cladodus neilsoni, 372, 373
Ctenacanthus, 373
Dinichthys, 196-199
Heterodontus francisci, 663, 681
H. galeatus, 663, 687
H. japonicus, 663, 693
embryonic, 744, 745, 746, 748
H. phillipi, 663, 665
H. quoyi, 676, 678, 679
Hybodus, 341-342
Notidanidae, 490
Symmorium reniforme, 372, 373
Squalus, 595, 601
pelvic,
Arthrodira, 198
Cestraciontidae, 695
Chlamydoselachus, 291-292, 340, 373-
377, 394-395, 434, 450, 541; VI-v
embryonic, 573, 594, 595, 601, 602,
604, 607, 610-612, 614-615
Cladoselache, 375
Dinichthys, 196-199
Heterodontus francisci, 681
H. japonicus, 663, 693, 713
embryonic, 744, 745, 747
H. phillipi, 665
Pleuracanthus, 341-342
radials in Chlamydoselachus, 376, 377, 378,
379, 380, 381
rays,
Chlamydoselachus, 294, 295, 340
Dinichthys, 197
Heterodontus japonicus, 746
Fin-fold theory, 341-342, 744, 745
Follicles, ovarian,
Bdellostoma, 49, 91, 95
Chlamydoselachus, 445, 546, 549
Heterodontus francisci, '703
Food,
Chlamydoselachus, 297
Dinichthys, 202
Heterodontus galeatus, 711
H. japonicus, 711
H. phillipi, 710
Fowler, H. W., see Jordan, D. 8.
Freminville, M., on Heterodontus quoyi, 660,
677, 678, 680
Bashford Dean Memorial Volume
Fraas, E., on Hybodus hauffmani, 660, 695
Firbringer, K.,
on Chlamydoselachus, 350, 358, 359, 362,
396, 398, 399
Heptanchus, 483
Galeocerdo tigrinus, 277, 678
ovaries and oviducts, 564
Galeus, pylorus, 405
Gambusia patruelis, 414-415
Ganoids, 722
Garman, 5.,
on Cephaloscyllium umbratile, 409
Cestracion, 658, 659, 663
Chlamydoselachus, 247, 249, 265, 272,
273, 277, 278, 279, 281, 283, 285, 286,
287, 288, 289, 290, 291, 293, 294, 296,
298, 299, 303, 305-206, 308, 309, 315,
335, 339, 340, 342, 343, 345, 350, 356,
358, 359, 360, 370, 373, 377, 380, 381,
385, 402, 410, 420, 433, 443, 446, 447,
458, 473, 475, 482, 490-491, 494, 532,
543, 550, 551, 569, 577, 579, 609
Heterodontus francisci, 681, 682, 684
H. galeatus, 687
H. phillipi, 660, 664, 665, 670, 674
H. quoyi, 677, 678, 680
H. zebra, 675
Heptanchus perlo, 409
Tsurus punctatus, 409
Gastrulation,
Bdellostoma, 56, 302
Chlamydoselachus, 539, 570, 484, 488-490
Heterodontus japonicus, 719, 720, 725, 729,
732-738, 739
H. phillipi, 717, 733, 735, 736, 737, 738
Torpedo, 738
Gegenbauer, C.,
on fin origin, 342
Heptanchus, 355, 363
Hexanchus, 351
Gemundia, 188
Gestation,
Chlamydoselachus, 302-303, 538-540, 556
Ginglymostoma, 533, 580
Gill, T. N.,
on Chlamydoselachus, 306-308, 335, 494
Heterodontus, 659
Gills,
Amphibia, 629
Arthrodira, 210
Cetorhinus, 277, 304
Chlamydoselachus, 260, 281, 339-340,
358-363, 371-373, 420-423, 429-430,
466-471, 593-595, 597-602,604-617,
626-629, 758; VI-v; VII41—VIliv
For details, see Chlamydoselachus,
gills
clefts,
Chlamydoselachus, 422, 429-430, 467,
468
Heterodontus japonicus, '742, 743, 744,
745,747, 752, 753, 760
covers,
Cetorhinus, 277, 302, 304
Chlamydoselachus, 281, 304, 339-340
Heterodontus, 679, 685, 693
Crossopterygii, 629
Dinichthys, 199-202
Dipnoi, 629
evolution of, 423
external in adult Chlamydoselachus, 629-
630
filaments,
Chlamydoselachus, 420-423, 429, 470,
623-630, 758, 759
Crossopterygii, 629
Dipnoi, 629
Heterodontus japonicus, 745-747, 758,
759
H. quoyi, 757, 758-759
Heptanchus, 423
Heterodontus francisci, 681, 683, 685
H. galeatus, 687
H. japonicus, 685, 693,755
embryonic, 742, 743, 744, 745, 746, 747,
752, 753, 755, 758, 759, 760; VU 1-1
H. quoyi, 678, 679, 685, 757
embryonic, 758-759
H. zebra, 676
openings (slits),
Arthrodira, 210
Chlamydoselachus, 260, 266, 314, 371-
373; Viv
Heterodontus francisci, 681, 683
H. galeatus, 687
H. phillipi, 669, 678
H. quoyi, 678
H. zebra, 676
phylogeny of, 423
Pliotrema, 339
Squalus, 594, 596, 600, 627, 628, 629
see also clefts above
Ginglymostoma cirratum, 564, 565, 576-581
cloaca, 561
egg, 301, 530, 561, 564, 573
blastoderm (disc), 582, 583, 590
blastula, 560
capsule (case), 530, 558, 560, 561, 568,
576-577, 579, 580-581,
tendrilliform processes, 579-581
gastrulation, 589
germinal disc, 589, 590
ovarian, 557, 564
plugs, 577, 579
size, 557, 563, 573, 576-577
wind, 558, 577, 580
yolk blastopore, 560
yolk mass, 533, 568, 577, 579
embryos, 301, 533, 560-562
perivitelline fluid, 530, 561, 577
Ginglymostoma cirratum—(continued)
gestation, 533, 565
gland, nidamental, 580, 581
ovaries and oviduct, 561, 564
ovoviviparity, 557, 573, 579
viviparity, 533, 580
Girard, C. F., on Heterodontus francisci, 681,
682
Girdles,
origin, 373, 376
pectoral,
Chlamydoselachus, 371-373
Cladodus, 372
Heptanchus, 370
Heterodontus, 661, 696
Hybodus, 372
Symmorium, 372
pelvic,
Arthrodira, 197, 198
Chlamydoselachus, 373-376; VI-v
shoulder, Cladoselache, 373
Glands,
in fins, 669
follicular, 669
nidamental,
Chlamydoselachus, 432, 433, 434, 445,
446, 448, 450-452, 543-544, 550-552,
554, 578-581
Ginglymostoma, 579-580
Heterodontus, '703
Scyllium, 447
pancreatic,
Chlamydoselachus, 413-415
Gambusia patruelis, 414-415
Heptanchus maculatus, 415
rectal,
Chlamydoselachus, 410-411
Heptanchus, 411
Heterodontus, 703
thyroid,
Amphioxus, 416
Chlamydoselachus, 415-418
Heptanchus, 418
Scyllium, 418
Gnathostomes, 67, 100, 357
Goodey, T.,
on Chlamydoselachus, 268, 350, 351, 355,
358, 359, 360, 362, 363, 366, 367, 368,
373, 376, 377, 380, 381, 388, 395, 396,
397, 415, 416, 425-426, 428, 453,487-
488, 624
Scyllium, 418
Goodrich, E. S.,
on Cestraciontidae, 569, 661, 670, 695
Chlamydoselachus, 291, 292, 343, 357,
422, 457, 482
Dinichthys, 145
Heterodontus, 684, 700
Scyllium, 455, 700
skull types, 699, 701
Analytical Subject Index
Squalus, 455
yolk sac, 756
Goto, on Chlamydoselachus, 448, 552
Gray, J. E., on Centracion, 658, 659, 665
Gregory, W.K.,
on body form, 338
Chlamydoselachus, 282, 283, 311, 340,
397, 398
Cladodus, 311
Pliotrema, 339
Grieg, J. A., on Chlamydoselachus, 255
Gudger, E. W., 43-62; 243-330; 521-646
on Chlamydoselachus, 336, 337, 342, 343,
345, 385, 401, 402, 420, 444, 449, 487,
498, 623, 624, 626, 629, 654, 751, 758
Elasmobranchii, 301
Ginglymostoma (original notes), 533,
534, 558, 560, 561, 564, 568, 576-577,
579, 580-581, 582, 590
Gunther, H.,
on Chlamydoselachus, 249, 250, 265, 267,
285, 291, 292, 293, 294, 350, 376,
377, 408, 409, 410, 411, 413, 450, 459
Heterodontus, 663
H. galeatus, 686, 687
H. quoyi, 677
Gyropleurodus, 657, 659, 676, 677, 686
G. galeatus, see Heterodontus galeatus
G. peruanus, see Heterodontus quoyi
Haswell, W. A.,
on Elasmobranchii, 582
Heterodontus phillipi, 712, 713, 716,
723, 731, 732, 733, 735, 736, 737, 738
Hawkes, O. A. M.,
on Chalamydoselachus, 273, 278, 288, 362,
392, 393, 394, 399, 403, 405, 406, 411,
413, 415, 419, 433, 434, 443, 446, 448,
449, 472, 474, 475, 477, 478, 484, 485,
486, 491, 492, 545, 546, 547, 549, 550,
551, 559, 562, 627
Heterodontus, 662
Head,
Arthrodira, 180, 200, 204, 205, 218
Asterolepidae, 132
Chlamydoselachus, 266-280, 396, 606, 625—
626; V-m
Coccosteus, 211
Dinichthys, 127-159, 189, 193, 194, 195,
211; [Vi—IV-m
Heterodontus, 678, 679, 685, 686, 699-700,
701
Lunaspis, 200
Macropetalichthys, 206
Scyllium, 476
Heart,
Chlamydoselachus, 457-461
Heterodontus, 742, 743, 744
Heptanchus, 461
Heintz, A., 115-224
on Acanthaspida, 157, 198
795
Arthrodira, 154
Dinichthys, 115-212
Heterostius, 134
Homostius, 169
spinal (plate), 177
Hermaphroditism,
Bdellostoma, 67-69, 76-78, 82, 83, 85, 86,
89, 95, 96, 98
Myxinoidea, 69-83, 88
Myxine, 70-76, 87, 88
Henle, J., see, Miiller, J.
Heptanchus maculatus, 336, 337, 338, 339
arches,
basibranchial, 363
branchial, 363
hyomandibular, 700
brain, 474-475
canal, sensory, 490, 492
circulatory system, 461, 464, 465, 467-468
aorta, 464
cranium, 351, 699, 700
dentition, 270, 311, 347
digestive system, 403, 407, 409
eye, 393
fins, 379-380
gill, 423
girdle, pectoral, 370
gland,
pancreatic, 415
rectal, 411
intestine, valvular, 409
jaw, 670
mesonephroi, 438
mesonephric ducts, 444
mouth, 270
muscles,
branchiomeric, 396
eye, 393
hypobranchial, 389
intermandibular, 399-400
trunk, 384, 385
myxopterygia, 395
nerves, 474-475, 483, 484, 485; VI-vi
notochord, 364, 366-367, 369, 683
ovaries and oviducts, 446, 449-450
palatoquadrate, 700
pelvis, 373, 375
pyloric vestibule, 403
reproductive system, 411, 441, 446, 449-
450
skeleton, 350
spiracles, 428
tail, 340
testes, 446
urinary sinus, 441
Heptranchias perlo, 409, 461
Heterodontidae, 651-784
afhnities to Hybodontidae ,694~702
arch, hyomandibular, 662
bibliography, 764-770
796
Heterodontidae—{continued)
classification, 657-664
collections of, see Collections above
color pattern, 663
cranium, 701
distribution, 661
embryology. 651
eye, 662
fins, 660, 663, 669
fossil, 664
girdle, pectoral, 661
gills, 662
hump, 660, 661, 662
jaw, 661, 699-700
nomenclature, 657-664
palatoquadrate, 662
sexual dimorphism, 702-705
spine, dorsal, 698
see also Cestraciontidae
Heterodontus (as 2 genus),
classification, 657-664
color pattern, 663
dentition, 662, 698, 761, 762, 763
eggs, 527
capsules, spiral flanges, 705-708
eye, 662
fins, 342, 663
head, 662, 686, 699-700, 701
hump, 660, 661, 662
phylogeny, 651
spiracles, 662
Heterodontus francisci, 654, 661
arch, branchial, 662
breeding season, 718
color pattern, 677, 681, 683. 684
cranium, 684, 699-700
dentition, 684
distribution, 664, 681, 683, 709-710
egg. 712
capsule, 707-708
ovarian, 702-703
embryo, 718-721
size, 718
spiracle, 681, 683
epigonal organ, 703
eye, 677
fins, 660, 663. 681, 683
gills, 681, 683
girdle, pectoral, 661, 696
gland, rectal, 703
head, 683, 685-686
hump, 683
jaw, 684, 699-700
mesentery, 703
nest, 713
notochord, 683
ovarian follicle, 703
ovanies and oviducts, 702-704
ridge, supraorbital, 679, 681, 683
scales, 684
Bashford Dean Memorial Volume
size, 679, 681, 682, 683, 684, 702
skeleton, 683
spine, dorsal, 681, 683
urogenital system, 702-705
Heterodontus galeatus, 660
breeding season, 712, 713. 717
color pattern, 687-688
dentition, 687, 688
distribution, 664, 686, 687
egg, 712, 713
capsule, 706-707, 715
tendrilliform processes, 706
fins, 663, 687
food, 711
gills, 687
head, 687
myxopterygia, 702
nasal openings, 687
nests, 713, 716
ridge, supraorbital, 687
size, 686
spawning, 713
spine, dorsal, 711
Heterodontus japonicus, 651-764
arch, mandibular, 662, 744, 745
bibliography, 764-770
brain, 735
embryonic, 740, 741, 742, 744. 745
breathing valve, 759
canal, :
neurenteric, 743
sensory, 746, 747
spiracular, 759
cloaca, 713
color pattern, 692, 693, 694, 702. 755. 756,
737
embryonic, 747, 748
dental ridge, 759
denticles,
dermal, 747, 755
oral, 760, 761
dentition, 691, 694, 711
anterior (cuspidate), 694, 763
development, 760-763
embryonic, 759
posterior (grinding), 694
rows, 694
distribution, 653, 664, 688-689, 709-710
eggs, 584, 689, 712, 723
discoidal, 728-732
furrows, 739; VII-va
holoblastic, 722, 724~725, 726-727,
749
lines, 724-728, 731, 732
total, 724-728
collecting, 631, 716
development, 703, 716, 717, 718, 739
disc, germinal, 719, 723, 725, 726, 728,
731, 733, 749; V4, VU, Viva
embryos on, 752, 753; VilL-vn
extrusion of, 713-714
gastrulation, 719, 720, 725, 729, 732-
738. 739; VIll1
mitosis, 729, 730, 731
nucleus, 729, 730, 731
ovarian, 703-705, 712, 728
polarity, 726-728
segmentation of, 728-732
size, 723-724
vitelline circulation, 748, 749, 750, 752,
753, 755, 756; VIll-v, Vivi
yolk,
blastopore, 739, 740, 748, 749, 750;
VIILv
mass, 733, 739, 741; VIL, VIIl-v
sac, 719, 746, 747, 748. 752, 756
stalk, 741, 744, 745. 750, 751; VII-v1
embryos, 527, 654, 689, 709, 717-751;
VIll-n, Vim
blood vessels, 720
brain, 740, 741, 742. 744. 745
branchial region, 746, 747
circulatory system, 720, 748, 749, 752,
753, 755, 756
color pattern, 747, 748
dentition, 759, 760-763
development, 651, 717-722, 740-748
ectoderm and entoderm, 734, 738, 739,
741, 742
eye, 741, 742. 743, 745, 746, 747.
fins, see below
flexures,
caudal, 743, 744
cephalic, 740, 741, 742. 744. 745. 746
cervical, 740, 741, 742, 743, 744
fold,
labial, 745, 746, 747
neural, 734, 740
blastoderm (disc), 582, 722, 729, 730,
731, 732, 733, 734, 738, 739. 741, 748,
749; VIll4, VIL, VIL-v
blastomeres, 725, 728. 729, 730, 731,
732
blastopore, 726, 738-740, 748, 749;
VIlL-v
blastula, 719, 729, 732. 733, 737, 738
capsule, 705, 707-709, 713-714, 715,
717, 720, 728, 752, 753; Vill-va
cleavage, 584, 653, 656, 724-732; VIIl1
gills, 742, 743, 744, 745. 746. 747. 752.
753, 758, 759, 760; VIll-m
grooves, 747
branchial, 742, 743, 744
pharyngeal, 744
gut,
fore, 734, 737
hind, 742, 743, 745
mid, 744
hatching of, 753, 720, 753
heart, 742, 743, 744
Heterodontus japonicus—embryos—(contd.)
jaw, 745, 761
mesoderm, 734, 740, 741, 742
myomeres, 744, 745, 746; VIILu,
Villain
neuromeres, 741
on egg, 752, 753; VII-vu
periblast, 733, 736, 738
phylogenetic significance, 722
pouch, Rathke’s, 759, 761
ridges, supraorbital, 746, 747
serial sections, 731
size, 720, 721, 739, 740, 741, 742, 745,
746, 747, 759, 760, 761, 762
somites, 734, 735, 740, 741, 742, 743,
744; VIII
spiracle, 742, 744, 745, 746, 747, 755,
757, 759
tail, 741, 742, 744, 746, 754
epigonal organ, 703
eye, 662, 694
embryonic, 741, 742, 743, 745, 746,
747
muscles, 742, 743
fins, 663, 752, 754; VUl-vu
anal, 663, 693
embryonic, 744, 745
caudal, 663, 693, 694
embryonic, 744, 745, 746, 755
dorsal, 663, 692-693
embryonic, 744, 745, 747, 748
pectoral, 663, 693
embryonic, 744, 745, 746, 748
pelvic, 663, 693, 713
embryonic, 744, 745, 747
fin folds, 744, 745
fin rays, 744, 745, 746
food, 711
gills, 755
cleft (embryonic) 742, 743, 744, 745,
747, 752, 753, 760
covers, 685, 693
filaments (embryonic), 745, 746, 747,
758, 759; VIL
glands,
nidamental, 703
rectal, 703
habits, 709, 710, 715
head, 683, 693
hump, 693
jaw, 711, 745, 761
mesentery, 703
mouth, 692, 711, 735
embryonic, 745, 746, 747, 759, 760
myxopterygia, 702
embryonic, 746, 747
nasal openings, 692
embryonic, 747
nest, 714-715, 716
nomenclature, 657-662, 688-693
Analytical Subject Index
colloquial, 689
notochord, 734, 735, 742
opisthure, 755
ovaries, 542-549, 703, 711-712
oviducts, 549-562, 703, 704, 714
palatoquadrate, 761
reproductive system, 542-563, 703-705
ridge, supraorbital, 692, 693, 694, 746, 747
embryonic, 746, 747
sexual dimorphism, 702
size, 685, 688, 690, 691, 692, 693, 694, 702,
756, 757
spawning, 712, 713-715, 716, 718
spines, dorsal, 689, 693, 747
spiracle, 692, 755, 757, 759
embryonic, 741, 742, 744, 745, 746, 747
tail, 754
embryonic, 741, 742, 744, 746, 754
venous system, 749, 750, 751; VIILv,
Vivi
venules, 749, 750, 751
young, 753-755, 756, 757, 758; VUll-vir
Heterodontus phillipi, 657, 658, 660, 661,
664-675, 677, 681, 688, 693
arch, branchial, 662
breeding season, 711-712
capsule, auditory, 700
color pattern, 666, 667, 668, 669
cranium, 699-700
dentition, 666, 670-675, 681
anterior (cuspidate), 671, 672, 674
embryonic, 672, 761
lower, 673, 674
number, 673
posterior (grinding), 671, 672, 674
rows, 672, 673, 674
upper, 673, 674
distribution, 664, 686, 689, 712, 713
egg, 731, 732
blastocoele, 736
blastoderm (disc), 582, 723, 731, 732,
733, 737, 738
blastula, 712, 717, 731, 732, 735, 736
capsule, 705-707, 712, 713, 725
cleavage, 716
lines, 731, 732
disc, germinal, 723, 731, 732
gastrulation, 717, 733, 735, 736, 737,
738
embryos and embryology, 712, 722-725,
731
dentition, 672, 761
ectoderm and entoderm, 737
periblast, 736
fin, 663
caudal, 666
dorsal, gland and spine, 669
pectoral, 663, 665
pelvic, 665
food, 710
797
gill slits, 669
head, 685
jaw, 670-675, 700
myxopterygia, 667, 702
nests, 712~713, 715, 716
nomenclature, 657-662, 664-674
notochord, 737
palatoquadrate, 760
reproductive system, 667
sexual dimorphism, 702
size, 665, 666, 667, 668, 669
Heterodontus quoyi, 654, 657-662, 686
color pattern, 676, 677, 678, 679, 680
dentition, 680-681
anterior, 680
rows, 681
distribution, 664, 676, 677
eye, 677, 679
fins, 663
anal, 676, 678
dorsal, 676, 678, 679
pectoral, 676, 678, 679
gills,
covers, 685
filaments (embryonic), 758-759
openings (slits), 678, 679
head, 678, 679
jaw, 680-681, 684
nasal openings, 679
ridge, supraorbital, 677, 678, 679, 683,
685
scales, 679
size, 676, 677, 678, 679, 684
skeleton, 678, 679
spines, dorsal, 679, 747
spiracle, 677, 678
Heterodontus zebra, 657-662, 663, 664
color pattern, 675
dentition, 676
distribution, 664, 675, 689, 693
fins, 663, 676
head, 685
ridge, supraorbital, 675
size, 675, 677
Heterostius, 134, 154, 180, 200
Hexanchus, 351
arch, basibranchial, 363
muscles, 399-400
neurocranium, 351
notochord, 352, 364
ovary, 446
see also Notidanus griseus
Hiyama, Y., see Kumada, T.
Hochstetter, F., on Acanthias, 455
Home, E., on elasmobranch eggs, 709
Homea burgeri, 48
Homostius, 132, 140, 141, 154, 169, 180, 192,
205
Howell, A. B., on Chlamydoselachus, 382,
383
798
Hussakof, L.,
on Arthrodira, 125, 180, 190, 191
Dinichthys, 116, 119, 121, 145, 149, 151,
160, 168, 169, 170, 173, 175, 184, 187
202, 208,
Huxley, T. H.,
on Heterodontus phillipi, 699-700
skull types, 699-700, 701
Hybodontidae,
affinities, 694-702
arch, neural, 696
dentition, 696, 697
fin, 696
jaw, 699
notochord, 696
spine (dorsal), 669
Hybodus, 660, 696, 699
cranium, 700, 701
dentition, 697
fins, 341-342
girdle (pectoral), 696
notochord, 494, 696
palatoquadrate, 700
spine (dorsal), 669
H. basanus,
arch, hyomandibular, 701
cranium, 701
jaws, 701
palatoquadrate, 700-701
H. delabechei, 697
H. dubrisiensis, 700, 701
H. hauffianus, 660, 695, 699, 700, 701
cranium, 699, 701
H. raricostatus, 697
H. reticulatus, 348, 349, 697
dentition, 348, 349
Hypoprion brevirostris, 565
H. signatus, 565
Ijima, I., 251, 657
Intestine, valvular
Cephaloscyllium umbratile, 409
Chlamydoselachus, 408-409, 412; VI-1v
Heptanchus maculatus, 409
Heptranchias perlo, 409
Isurus punctatus, 409
Raja, 409
Scyllium canicula, 409
Zygaena, 409
Tsurus punctatus, 409
Ito, K. (artist), 253, 268, 295, 675, 993
Jaekel, O.,
on Arthrodira, 125, 142, 153, 185, 187,
197, 200, 201
Coccosteus, 143, 144, 175, 177, 199
Dinichthys, 152, 175, 180, 181, 184, 190
Hybodus hauffianus, 699, 700, 701
Pholidosteus, 134, 151, 175
Synosteus, 205
Bashford Dean Memorial Volume
Jaekel-Adams theory, 185, 187
Jagorina, dentition, 206
Jansen, J., on Myxine glutinosa, 99
Japanese Bullhead Shark, 664, see Hetero-
dontus japonicus
Jaw,
Antiarchi, 187
Arthrodira, 145, 184-185, 187, 207
Cestraciontidae, 699
Chlamydoselachus, 268, 269, 272, 353, 354,
356, 358, 484
Coccosteus, 185, 187
Dinichthys, 118, 121, 138-155, 184, 185,
187, 188, 189, 190; [V-vir
Heptanchus, 670
Heterodontidae, 661, 699-700
Heterodontus francisci, 684, 699-700
H. japonicus, 711, 745, 761
H. phillipi, 670-675, 700
H. quoyi, 680-681, 684
Hybodontidae, 699
Hybodus basanus, 701
Scyllium, 700
Johnson, S. E., on Mustelus, 492
Johnston, J. B., on occipitospinal nerve, 483
Jordan, D. S.,
on Chlamydoselachus, 265, 273
Heterodontidae, 659, 660
Heterodontus francisci, 681
H. japonicus, 679
Kemna, A., on gills, 199
Kidneys, see Mesonephroi
Klein, J. T., on Cestracion, 658, 659
Koenen, A. von,
on Arthrodira, 180, 197
Coccosteus, 176
Dinichthys, 197, 198
Kumada, T., and Hiyama, Y.,
on Heterodontus francisci, 681, 682, 683
H. quoyi, 677
Kupfer, C. von, on Bdellostoma, 98, 99
Kuwabara, I. (artist), 530, 656
Lacépede, B., on Heterodontus, 654
Lacerta, 389
Lamna cornubica, 574-575
eggs, 574; size, 575
embryo, 574, 575
reproductive system, 578
Lawley, R., on Chlamydoselachus, 311-312,
348
Leigh-Sharpe, W. H.,
on Chlamydoselachus, 348
Heterodontus, 702
myxopterygia, 376, 395, 451, 452, 453,
472, 542, 702
Lepidosiren, 389
Lepidosteus, 394, 726, 728
Leriche, M., on Chlamydoselachus tobleri, 348
Lesson, R. F., on Heterodontus phillipi, 665,
666, 677, 681
Leydig, F.,
on blastoderms, 582
Squalus acanthias, 620
Lohberger, J., on egg of Lamna, 575
Loppe, E., see, Pellegrin, J.
Lozano Rey, L., on Chlamydoselachus, 256,
266, 273
Lunaspis heroldi, 199, 200
Lungfish, 722
Luther, A. F.,
on Chlamydoselachus, 399
Heptanchus, 399
M Coy. F..,
on Dinichthys, 145
Heterodontus phillipi, 659, 664, 667.
670, 673, 674, 705, 710, 711
Placodermata, 202, 209
Maclay, N. and Macleay, W.,
on Heterodontidae, 657, 658, 659, 660,
663, 670
Heterodontus francisci, 681, 682, 685
H. galeatus, 686, 687, 688, 711
H. japonicus, 689, 690, 691
H. phillipi, 664, 666, 667, 668, 671, 673,
674, 702
H. quoyi, 677
H. zebra, 675, 676
Macleay, W., see above
Macropetalichthys, 193, 194
armor, 204
canal, sensory, 206
carapace, 206
phylogeny, 204, 206
Marshall, A. M., on Elasmobranchs, 391,
742
Maurer, F., on Chlamydoselachus, 382, 384
Medlen, A. B., see Potter, G. E.
Mertens, R., on Chlamydoselachus, 253, 265,
282, 295
Mesentery,
Chlamydoselachus, 437, 438, 439, 440, 442,
443, 445, 447
Heterodontus, 703
Mesonephroi,
Bdellostoma, 90, 98
Chlamydoselachus, 432, 433, 434-438
Heptanchus, 438
Myxinidae, 441
Mesopterygium, see Girdle, pectoral
Mesovaria,
Chlamydoselachus, 432
Myzxine, 70, 90, 91
see also Mesentery
Miller, H.,
on Arthrodira, 197, 199, 208
Coccosteus, 145
Dinichthys, 184, 187
Mivart, St.G., on fin folds, 341
Momose, F., on Chlamydoselachus, 535, 543,
546, 547
Moodie, R. L., on Dinichthys, 145, 146
Mouth,
Arthrodira, 187-192
Cetorhinus, 339
Chlamydoselachus, 267-269, 295, 338-
339, 593-597, 599-602, 604, 605,
607-616, 623-625; V-11
Dinichthys, 187, 189-190
Heptanchus, 270
Heterodontus japonicus, 292, 711, 745, 746,
747, 755, 759, 760
Teleostomi, 338, 339
Miller, J., and Henle, J.,
on Heterodontus, 666, 688, 689
Myzxine, 69, 70, 71
Munro, A., on Raja, 455
Murphy, R. C., see Nichols, J. T.
Muscles,
Acanthias, 390, 394
Amia, 394
Arthrodira, 194
Cestracion, 394
Chlamydoselachus, 381-400, 484, 485;V Liv
For details see, Chlamydoselachus,
muscles
Coccosteus, 190
Dinichthys, 188, 189-191,
For details see, Dinichthys, muscles
Elasmobranchii, 391, 394, 742, 743
Heptanchus, 384, 385, 389, 390, 391, 393,
395, 396, 399-400
Hexanchus, 399-400
Lacerta, 389
Lepidosiren, 389
Lepidosteus, 394
Scyllium, 389, 392, 394
Scymnus, 389
Selachii, 391
Squalus, 389
Teleostomi, 394
Mustelus,
canal, sensory, 492
ear, 355
fin, dorsal, 379
Mylostoma, dentition, 186
Myomeres,
Chlamydoselachus, 382, 383, 388, 593, 624
Heterodontus japonicus, 744, 745, 746;
Villian
Squalus, 383
Myotomes,
Chlamydoselachus, 388-389
Lacerta, 389
Lepidosiren, 389
Petromyzon, 389
Protopterus, 389
Scyllium, 389, 476
Squalus, 389
Analytical Subject Index
source of hypobranchial muscles, 388
Myxine,
corpora lutea, 90, 97
distribution, 72, 73, 75
ducts, 441
eggs, 74, 75, 90
hermaphroditism, 70, 75, 76, 77, 78
mesorchia, 70, 78, 83, 84
mesovarium, 70, 90, 91
ovary, 90
phylogeny, 99
reproductive system, 70, 75,77
sex, 72, 73, 74
spawning, 93, 94, 96
spermatogenesis, 73, 85
spermatozoa, 72. 74, 76
testis, 70, 75, 77
Myxine glutinosa, 69, 79, 89, 91, 99
hermaphroditism, 70-76
mesorchium, 70
mesovarium, 70
ovary, 70, 72, 74, 90
Myxinidae, mesonephric ducts, 441
Myxinoidea, 47-62, 67-69, 97-100
age, 92
cartilage, labial, 357
classification, 69
egg, 88-91
embryo, 68
feeding habits, 69
parasitic, 69
phylogeny, 97-100
reproductive system, 67-75, 78-87; II]4,
Ilav
spawning, 67, 93, 94, 96
Myxopterygia,
Arthrodira, 724
Bdellostoma, 92
Chlamydoselachus, 291, 292, 295, 298, 373,
376-377, 395, 451-454, 472, 541, 542,
624; V-v; VI-v
Cladoselache, 724
Elasmobranchii, 531
Heptanchus, 395
Heterodontus, 702
H. galeatus, 702
H. japonicus, 702, 746, 747
H. phillipi, 667, 702
Nansen, F.,
on hermaphroditism, 78
Myxine, 72, 73, 74, 75,76, 93
Nasal organs,
Chlamydoselachus, 207, 279, 503, 593, 599.
600-602, 604 607-617
Heterodontus galeatus, 627
H. japonicus, 602, 747
H. quoyi, 679
Neal, H. V.,
on muscles, 389, 391
799
somites, 735
Necturus,
brain, 99
egg, 726
Nerves,
Chlamydoselachus, 368, 472-487; VI-vu
For details see, Chlamydoselachus,
nerves
Heptanchus, 474, 475, 483, 484; VIl-vu
Raja, 487
Spinax, 483
Squalus, 484, 487
Torpedo, 484
Nests,
Heterodontus japonicus, 712-715, 716
H. phillipi, 712-713, 715, 716
Neurocranium,
Arthrodira, 192-194
Chlamydoselachus, 350, 351
Dinichthys, 192-196
Hexanchus, 351
primordial, 192-196
Newberry, J. 5.,
on Acanthaspis, 176
Arthrodira, 180, 187, 202, 208
Cephalaspidae, 176
Dinichthys, 115, 117, 118, 119, 127, 135,
160, 166, 169, 170, 175, 179, 184, 190,
195, 197, 198
Nichols, J. T., and Murphy, R. C.,
on Heterodontus quoyi, 678
Nishi, $., on Chlamydoselachus, 392
Nishikawa, T., on Chlamydoselachus, 250,
257, 265, 299, 300, 302, 445, 448, 528,
529, 555, 567, 573, 582, 583, 585, 586,
587, 588, 591, 593, 598, 619
Norris, H. W., on Squalus, 492
Notidanidae,
canal, sensory, 490
dentition, 673
ear, membranous labyrinth, 487-488
fin, pectoral, 490
Notidanus (Hexanchus) griseus, 488
Notochord,
Chlamydoselachus, 351, 352, 363-370,
494
Heptanchus, 364, 366, 367, 369, 683
Heterodontus francisci, 683
H. japonicus, 734, 735, 742
H. phillipi, 737
Hexanchus, 52, 364
Hybodontidae, 494, 696
Notorhynchus, 468
Obrutschew, D. W.,
on Angarichthys, (spinal plate), 177
Dinichthys, 145
Ogilby, J. D.,
on Heterodontus, 659
H. galeatus, 688
800
Opisthure, 755
Orodontidae, 695
Orodus, 696, 697, 699
Osburn, R. C.,
on Chlamydoselachus, 342, 376, 592
Heterodontus francisci, 709
Osorio, B., on Chlamydoselachus, 256
Ostracoderms, 99
Ovarian follicles, see Follicles, ovarian
Ovary,
Bdellostoma, 86, 88, 89, 91, 92; IlI1
Carcharhinus, 564, 565 :
Chlamydoselachus, 299, 432, 433, 445, 446, |
447, 535, 543, 544-547
Galeocerdo, 564
Ginglymostoma, 564
Heptanchus, 446
Heterodontus francisci, 702-703
H. japonicus, 542-549, 703, 711, 712
Hexanchus, 446
Myxine glutinosa, 70, 72, 74, 90
Pteroplatea maclura, 565-566
Oviducts,
Carcharhinus obscurus, 564, 565
C. platyodon, 564, 565
Chlamydoselachus, 293, 299, 302, 431, 432,
433, 434, 435, 437, 445, 446-450, 543,
544, 549-550, 558, 559, 562, 563
Elasmobranchii, 301, 549, 565-566
Galeocerdo, 564
Ginglymostoma, 564
Heptanchus, 449-450 |
Heterodontus francisci, 702 |
H. japonicus, 549-562, 703, 704, 714
Pteroplatea maclura, 565-566
Oviparity, 300, 301, 531-533, 578, 579, 580
Ovoviviparity, 301, 531-533, 578, 579, 580
see also Viviparity
Oxyrhina, egg and embryo, 576
Oyster-crusher, 664, see Heterodontus phillipi
Palaeospondylus, 11, 67
Palatoquadrate,
Cestraciontidae, 695-696
Chlamydoselachus, 353, 354, 356, 358, 424,
425
Heptanchus, 700
Heterodontidae, 662
Heterodontus japonicus, 761
H. phillipi, 760
Hybodus basanus, 700-701
sharks, 699
Paleospinax, 696-698
dentition, 698
denticles, 698
spine, dorsal, 698
Palmen, J. A., on Chlamydoselachus, 255
Pancreas, see Glands, pancreatic
Pander, C. A.,
on Arthrodira, 163, 180, 192, 208
(
Bashford Dean Memorial Volume
Coccosteus, 175
Dinichthys, 184
Placoderms, 145
Parker, T. J.,
on Raja, 409
Scyllium canicula, 409
Zygaena, 409
Patten, W., on Dinichthys, 184, 187, 199,
208
Pellegrin, J., and Loppé, E., on Chlamy-
doselachus, 255
Pelvis,
Chlamydoselachus, 373-376
Heptanchus, 373, 375
Perivitelline fluid, 561
Petromyzon,
mesonephric ducts, 441
muscles, 389
Phillip, A., on Heterodontus phillipi, 664, 670
Phlyctaenaspis, 127, 134, 141, 142, 148, 175,
177, 205
P. acadica, 134
Pholidosteus, 134, 144, 151, 175,177
spinal (plate), 177
Pigfish, 664, see Heterodontus phillipi
Placodermata, 9, 145, 202, 209-211
canals, sensory, 209, 210, 211
Plagiostomes, eye-stalks, 355
Pleuracanthus, 341-342
dentition, 310
fins, 342
P. laevissimus, 310
Pliotrema, gills, 339
Pollard, H. B., on labial cartilage, 357
Potter, G. E., on Gambusia patruelis, pan-
creas, 414
Pouch, Rathke’s, 759, 761
Price, G. E.,
on Bdellostoma, 93, 94, 98
Myzxinoidea, 98
Pristiurus melanostomum, 582
egg,
blastoderm (disc), 582, 589, 748, 749
blastopore, 748, 749
blastula, 731
cleavage, 589
germinal area, 589
germinal disc, 723, 727
vitelline circulation, 748-749
yolk: mass, 748; sac, 756; stalk, 748
embryo, 722, 748, 750
arterial ring, 749
arterioles, 749, 751
Protoplasm, 52, 53, 56, 57
Protopterus, 389
Pteroplatea maclura, 565—566
Pterygoquadrate, see Palatoquadrate above
Putnam, F. W., on Myxine, 93
Pylorus,
Chlamydoselachus, 405-406, 412;
vestibule of, 404-405, 412
Galeus, 405
Heptanchus, vestibule of, 403
Radcliffe, L., see Evermann, B. W.
Raia batis, 621
Raja,
canals,
pericardio-peritoneal, 455
sensory, 455
intestine, valvular, 409
nerve, spinal, 487
yolk sac, 756
R. laevis, 487
Reconstruction,
Arthrodira, 122, 123, 142
Bdellostoma, egg, 47
Dinichthys, 117-122, 142, 143, 145, 151,
152, 153, 159, 160, 161, 168, 169, 174,
180, 188-189, 191, 192, 202, 203
Regan, C. T.,
on Cestraciontidae, 695
Heterodontidae, 657, 659, 663
Pliotrema, 339
Reproductive system,
Bdellostoma, 83-88, 90, 95; I1]1—IIL1v
Chlamydoselachus, 412, 431-455, 541-564;
Viv
Elasmobranchii, 547
Heptanchus, 411, 441, 449-450
Heterodontus francisci, 702-705
H. japonicus, 542-563, 703-705
H. phillipi, 667
Lamna, 578
Myxine, 67-75, 78-87; I111—Il1v
see also Ovary, Oviduct, Testes, Uterus
Respiratory system,
Arthrodira, 199-202, 207
Chlamydoselachus, 267, 279-281, 339-340,
359, 419-431, 467-472, 593-595, 596,
597-602, 604-617, 625-630, 758;V-n,
Vav; Vilu, Vila, Viliv
Heterodontus japonicus, 692, 741, 742, 743,
745, 746, 747, 752, 753. 755, 757, 758,
759; Vila
H. phillipi, 665, 666, 667, 668, 669
H. quoyi, 677, 678, 685, 758-759
Selachii, 743
Squalus, 594, 596, 600, 601, 627, 628, 629
Rhineodon typus, 277
Richards, A., on egg chromosomes, 731
Ridge, supraorbital,
Heterodontus francisci, 679, 681, 683
H. galeatus, 687
H. japonicus, 692, 693, 694, 746, 747
H. quoyi, 677, 678, 679, 683, 685
H. zebra, 675
Rose, C., on Chlamydoselachus, 248, 286,
298, 342, 346, 591
Roule, L., on Chlamydoselachus, 254, 255
Riickert, J., on blastula, Pristiurus, Torpedo,
731
Sanzo, L., on Carcharodon rondeletii, 575, 5'76
SavilleKent, W., on Heterodontus phillipi,
661, 664, 665, 668, 669, 710
Scales,
Acanthaspida, 210
Chlamydoselachus, 286, 287, 288, 294,
342-350
Heterodontus francisci, 684
H. quoyi, 679
placoid, see Denticles, dermal
Scammon, R. E., on Squalus, 468, 585, 593,
733, 742
Schreiner, A., and K. E., on Myxine, 73, 75,
76, 88, 91, 94
Sclerotic ring,
Arthrodira, 206
Coccosteus, 211
Dinichthys, 158-159
Placodermata, 209
Macropetalichthys, 206
Scoliodon terraenovae, 565
Scyllium,
canal, pericardio-peritoneal, 455
cranium, 699, 700
egg,
blastoderm, 729
cleavage, 729
embryo, 476, 722
gland, nidamental, 447
jaw, 700
muscles,
appendicular, 394
hypobranchial, 389
myotomes, 389
Scyllium canicula,
arches, visceral, 476
embryo, 476
hatching of egg, 540
intestine, 409
muscles, 389, 392
eye, 392
myotomes, 476
thyroid gland, 418
Scyllium catulus, 540, see Squalus catulus
Scymnus,
cranium, 351
muscles, hypobranchial, 389
Seabra, A. F. de, on Chlamydoselachus ang-
uineus, 256
Selachii,
arches, gill and pharyngeal, 743
canal, pericardio-peritoneal, 455
embryo, 742
muscle, eyeball, 391
respiratory system, 743
Selenosteus, 158
Semper, C., on Hexanchus, 446
Analytical Subject Index
Sewertzoff, A. N.,
on labial cartilage, 357
paired fins, 372
Sex,
Bdellostoma, 70, 77-78, 82, 83, 85, 86, 89,
95, 96
Ginglymostoma, 560
Heterodontus francisci, 681, 682, 683, 684,
702
H. japonicus, 690, 691, 692, 693, 694, '702
H. phillipi, 669, 681, 702
H. zebra, 675, 676
Myxine, 72, 73, 74
Shagreen, 278, 286, 695
Shann, E. W., on Lamna cornubica, 574
Shark,
Bulldog, 664, see Heterodontus phillipi
Bullhead, 660-661, see Heterodontidae
chrondocranium, 699
Hammerhead, 658, 659, see Zygaena
Japanese Bullhead, 664, see Heterodontus
japonicus
Nurse, see Ginglymostoma
palatoquadrate, 669
Port Jackson, 664, see Heterodontus phillipi
Tiger, see Galeocerdo
Siebold, P. F., on Heterodontus japonicus,
688, 689, 690
Size,
Bdellostoma, 82, 98
Chlamydoselachus, 248, 252, 254, 255, 256,
260-265, 273, 274, 279, 281, 282, 283,
290, 295, 444, 546, 578, 662, 663
Heterodontus francisci, 679, 681, 682,
683, 684, 702
H. japonicus, 685, 688, 690, 691, 692, 693,
702
H. phillipi, 665, 666, 667, 668
H. quoyi, 676, 677, 678, 679, 684
H. zebra, 675, 677
Skeleton,
calcification, 350
Chlamydoselachus, 350-380, 390, 494;
Via, Vian
visceral, 200, 355, 356-364; VI-n, VI-m
Dinichthys, 192, 196, 199
Heptanchus, 350
Heterodontus francisci, 683
H. quoyi, 678, 679
Smith, B. G., 43-62: 243-330; 331-520; 647-
784
on Chlamydoselachus, 335, 336, 337, 342,
343, 345, 385, 401, 402, 420, 444, 449,
487, 492, 542, 544, 546, 557, 559, 561,
591, 595, 623, 624, 626, 627, 630, 744,
758, 759
Cryptobranchus, 728, 739
Squalus, 627, 628, 629
Somites,
Chlamydoselachus, 388
801
Elasmobranchii, 742, 743
Heterodontus japonicus, 734, 735, 740, 741,
742, 743, 744; VU
Heterodontus japonicus, 734, 735, 740, 741,
742, 743, 744; VIL
Squalus, 735, '740
Snyder, J. O., see Jordan, D. S.,
Speidel, C. C., on Squalus acanthias, 487
Spermatogenesis, 73-74, 76, 85
Spinal (plate),
Acanthaspis, 176, 177
Angarichthys, 177
Arthrodira, 176, 179
Coccosteus, 176, 177, 210
Dinichthys, 159, 172, 174, 176-179, 198;
1V-x
Pholidosteus, 177
Spine,
dorsal,
Cestraciontidae, 696
Heterodontidae, 698
Heterodontus francisci, 681, 683
H. galeatus, 711
H. japonicus, 689, 693, 747
H. quoyi, 679, 747
Hybodontidae, 669, 696, 698
Paleospinax, 698
Squalus, 669
Synechodus, 698
pectoral, Dinichthys, 198-199
Spinax,
nerves, occipital, 483
yolk sac, 756
Spiracle,
Chlamydoselachus, 279-281, 340, 423-430;
Va
embryonic, 423-430, 596, 598, 599-602,
604, 607-608, 610-613, 615
Elasmobranchii, 340, 428
Heptanchus, 428
Heterodontus francisci, 681, 683
H. japonicus, 692, 755, 757
embryonic, 741, 742, 744, 745, 746,
747
H. phillipi, 665, 666, 667
H. quoyi, 677, 678
Hexanchus, 428
Squalus, 487, 600
Squatina, 340, 427
Spleniale (plate), 185
Squalus acanthias,
canal,
pericardio-peritoneal, 455
sensory, 489-490, 492
circulatory system, 620:
aorta, 464, 465
arteries, 468
ducts, 441
egg, 585
blastoderm, 585, 733
802
Squalus acanthias—(continued)
embryo, 593, 594, 595, 601, 627. 628, 629,
22, 734, 742
myomeres, 383
somites, 735, 740
spiracle, 487, 600
fins,
dorsal with spine. 669
pectoral (embryonic), 595, 601
gills (embryonic), 594, 596, 600, 627, 628,
629
glands,
follicular, 669
of dorsal spine, 669
muscles, 389
nerves,
occipitospinal, 484
spinal. 487
Squalus catulus, hatching of eggs, 540
S. sucklit, mesonephric ducts, 444
Squatina, spiracle, 340, 427
Stead, D. G., on Chlamydoselachus, 257
Steindachner, F., on Chlamydoselachus, 248
Stensio, E. A.,
on Arthrodira, 126, 146, 184, 187, 206, 208
Dinichthys, 148, 176, 178, 187, 188
Macropetalichthys, 193, 204, 205
Ostracoderms, 99
Phlyctaenaspis, 141, 142, 148
Stetson, H.,
on Arthrodira, 208
Dimichthys, 122, 145, 148, 154, 159, 191.
194, 195, 199
Stewart, C., on Notidanus (Hexanchus)
griseus, 488
Stockard, C. R., on Bdellostoma, 99
Stomach,
Chlamydoselachus, 403-404
Heptanchus, 403
Striver, J., on Heterodontus phillipi, 659,
666, 671, 672
Symmorium renijorme, 372-373
girdle, pectoral, 372
Syncytium, 733, 736, 738
Synechodus, 696
cranium, 701
dentition, 697-698
spine, dorsal, 698
Synosteus, 205
Tabbigaw, 664, see Heterodontus phillipi
Tail,
Cestraciontidae, 696
Chlamydoselachus, 248, 249, 250, 288, 289,
290, 293, 364. 369-370, 624-625
embryonic, 296, 593, 594, 598, 601, 604,
607. 611-614, 617, 620-621
Heptanchus, 340
Heterodontus japonicus, 754
embryonic, 741, 742, 744, 746, 754
Tee-Van, J., see, Beebe, W.
Teleostomi, 201, 339
mouth, 338, 339
muscle, appendicular, 394
Testis,
Bdellostoma, 70, 83-85, 89; II
Cestraciontidae, 696
Chlamydoselachus, 450
Heptanchus maculatus, 446
Myxine, 70-75, 7
Thacher, J. K., on fin-fold theory, 341
Thyroid, see Gland, thyroid, above
Titanichthys, 140, 166
Torpedo ocellatus,
blastoderm (disc). '733, 739
blastula, 731
gastrula, 734
nerve, occipitospinal, 484
Townsend, C. H., on Heterodontus, 683
Traquair, R. H.,
on Arthrodira, 125, 180, 187, 195, 197,
199, 200
Coccosteus, 143. 168, 169, 176
Dinichthys, 144, 184
Phlyctaenaspis, 134
Trautschold, H. von, on Arthrodira, 197
Triakis semifasciatus, dentition, 345
Vaillant, L., on Oxyrhina, 576
Valenciennes, A., on Heterodontus quoyi,
660, 676, 677
Van Wijhe, J. W..
on Scyllium, 382, 392
Selachii, 391. 742
Vertebral column,
Chlamydoselachus, 363, 364-366, 367.
368-370. 436
Coccosteus, 196, 197
Dinichthys, 196-199
Vetter, B., on Heptanchus, 390, 399
Viviparity,
Chlamydoselachus, 298-301, 528, 331-534,
542, 559
development from ovoviviparity, 580
Elasmobranchii, 301
Ginglymostoma, 533, 580
Vitelline circulation, see under Embryo above
Waite, E. R..
on Heterodontus galeatus, 660, 687, 688,
706, 707, 712, 713
H. phillipi, 668, 669, 705, 706, 712
Weber, M., on Myxine, 71, 93
White, E. G.. on Chlamydoselachus, 253, 274
Whitley, G. P.,
on Heterodontus galeatus,686,687 688.717
H. phillipi, 660, 669. 710, 712
Wilder, B. G., on Chlamydoselachus, brain,
473. 474
Woodward, A. 5.,
Bashford Dean Memorial Volume
on Acanthaspis, 177
Acrodus, 697
Arthrodira. 125, 163, 180, 187, 197. 199,
202
Cestraciontidae, 695, 696, 699
Chlamydoselachus, 335, 342
Coccosteus. 143, 199
Dinichthys, 122, 170, 173, 184, 192
Heptanchus, 700
Heterodontus, 659
Hybodontidae, 494, 696, 697, 699, 700,
701, 702
Wright, A. A., on Dinichthys, 119, 170, 173
Wyman, J., on Raia batis, 621
Yatsu, N. (artist), 656, 657
Yolk,
blastopore,
Cryptobranchus, 739
Heterodontus japonicus, 739, 740, 748,
749, 750; Villav, VIIL-v
cord, 301; VIL-n
mass,
Chlamydoselachus, 572; VIL-v
Ginglymostoma, 577, 579
Heterodontus japonicus, 733, 739, 741;
Villa, VIIL-v
Pristiurus, 748
sac,
Chlamydoselachus, 300. 301, 303, 449
533, 555-557, 559, 571, 573, 576, 595,
596. 602, 603, 610, 612-621, 627;
Vila
Elasmobranchii, 301
Heterodontus japonicus, 719, 746, 747.
752, 756
Pristiurus, 756
Raja, 756
Spinax, 756
stalk,
Chlamydoselachus, 593, 595, 597, 602,
603, 605, 610, 612, 614, 615, 618-621
Heterodontus japonicus, 741,°744, 745,
750, 751; Vivi
Pristiurus, 748
syncytium, 733, 736, 738
vascular system,
Chlamydoselachus, 620-622; VIL-v
Felichthys, 622
Ziegler, H. E.,
on Chlamydoselachus, 303, 592, 596, 627
Torpedo ocellatus, 733, 734. 739
Zittel, K. A. von,
on Arthrodira, 202, 208
Cestraciontidae, 651, 696
Heterodontus, 659, 660
Hybodontidae, 696
Zygaena, 409, 658
intestine. 409
eRe he
BASHFORD DEAN MEMORIAL VOLUME
ARCHAIC FISHES
Edited By
_ EUGENE WILLIS GUDGER
Articte VI
THE ANATOMY OF THE FRILLED SHARK
CHLAMYDOSELACHUS ANGUINEUS Garman
By BERTRAM G. SMITH
Professor of Anatomy
New York University College of Medicine
New York City
AOI
Ot Ce,
<1
NEW YORK
PUBLISHED BY ORDER OF THE TRUSTEES
Issued December 22, 1937
5
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Meare NENA at
THE BASHFORD DEAN MEMORIAL VOLUME
ARCHAIC FISHES |
EDITED BY EUGENE WILLIS GUDGER
Published by The American Museum of Natural History
New York City
*
Article No. I. Mezmortat or Basrorp Dean, sy W.K, Grecory. 1930, pp. 1-42, 8 half—tone plates
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Article No. Il. Tue SEGMENTATION OF THE Ecc Or THE Myxinorp, Bdellostoma stouti, BASED ON THE
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Price $2.50
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The Dean Memorial Volume will probably be completed with two more articles. Title page with
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THE
~BASHFORD DEAN MEMORIAL VOLUME
ARCHAIC FISHES
Edited By
EUGENE WILLIS GUDGER
Articie VIL
THE BREEDING HABITS, REPRODUCTIVE ORGANS
AND EXTERNAL EMBRYONIC DEVELOPMENT
OF CHLAMYDOSELACHUS, BASED ON NOTES
AND DRAWINGS BY BASHFORD DEAN
By E. W. GUDGER
Honorary Associate in Ichthyology
American Museum of Natural History.
oP SO
NEW YORK
PUBLISHED BY ORDER OF THE TRUSTEES
Issued October 15, 1940
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ee
ai Mare i
ee
Le
ro S
THE BASHFORD DEAN MEMORIAL VOLUME
ARCHAIC FISHES
EDITED BY EUGENE WILLIS GUDGER
Published by The American Museum of Natural History
New York City
Article No. I. Memoria or Basurorp Dzan, By W. K. Grecory. 1930, pp. 1-42, 8 half-tone plates
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Article No. I]. Tue Sz¢MenraTION OF THE Ecc or THE Myxtnom, Bdellostoma stouti, BAssD ON THE _
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Price $2.50 i
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Article No. VI. THe Anatomy OF THE FRItLED SHARK, Chlamydoselachus anguineus, BY BERTRAM
G. Smirx. 1937, pp. 331-520, 7 half—tone plates, 128 text—figures. Price $3.50.
Article No. VII. Tue Breepinc Hasits, RepropuctivE ORGANS AND ExTERNAL EMBRYONIC DEVEL-
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a>
The Dean Memorial Volume will be combed with one more Article, No. VIII, on the Bee
ology of the Japanese bullhead shark by Dr. B. G. Smiru.
A title page, introduction, table of contents and an index will be furnished when the Volume
is completed.
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THE
BASHFORD DEAN MEMORIAL VOLUME
ARCHAIC FISHES
Edited By
EUGENE WILLIS GUDGER
Articie VII
THE HETERODONTID SHARKS:
_ THEIR NATURAL HISTORY, AND THE EXTERNAL
_ DEVELOPMENT OF HETERODONTUS JAPONICUS
BASED ON NOTES AND DRAWINGS
BY BASHFORD DEAN
By BERTRAM G. SMITH
Professor of Anatomy
New York University College of Medicine
New York City
NEW YORK
PUBLISHED BY ORDER OF THE TRUSTEES
Issued October 1, 1942
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